The importance of appropriate initial bacterial colonization of the intestine in newborn, child, and adult health

Pediatric Research

Volumn 82, Issue 3, 2017, Pages 387-395

  Walker, W Allan ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PREBIOTIC AGENT; PROBIOTIC AGENT;

ADAPTATION; ADULT; BACTERIAL COLONIZATION; CHILD; DIET; DYSBIOSIS; FECAL MICROBIOTA TRANSPLANTATION; HOST RESISTANCE; HUMAN; INTESTINE FLORA; METABOLISM; NEWBORN; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYMBIOSIS; BACTERIUM; BREAST FEEDING; FEMALE; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION;

ADULT; BACTERIA; BREAST FEEDING; CHILD; DYSBIOSIS; FECAL MICROBIOTA TRANSPLANTATION; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; INFANT, NEWBORN;

EID: 85028357647     PISSN: 00313998     EISSN: 15300447     Source Type: Journal    
DOI: 10.1038/pr.2017.111     Document Type: Review

References (105)

1. Rautava S, Luoto R, Salminen S, et al. Microbial contact during pregnancy, intestinal colonization and human disease. Nat Rev Gastroenterol Hepatol 2012; 9: 565-76.
2. Shanahan F. Host-flora interactions in inflammatory bowel disease. Inflamm Bowel Dis 2004; 10: S16-24.
3. Renz H, Brandtzaeg P, Hornef M. The impact of perinatal immune development on mucosal homeostasis and chronic inflammation. Nat Rev Immunol 2012; 12: 9-23.
4. Martin CR, Caicedo RA, Walker WA. Development of intestinal mucosal barrier. In: Neu J, ed. Gastroenterology and Nutrition: Neonatology Questions and Controversies. St Louis, MO: Elsevier/Saunders, 2012: pp 39-58.
5. Alenghat T, Osborne KC, Saenz SA, et al. Histone deacetylase 3 coordinate commensal-bacteria-dependent intestinal homeostasis. Nature 2013; 504: 153-7.
6. Zilbauer M, Zellos A, Jenke A, et al. Epigenetics in paediatric gastroenterology, hepatology, and nutrition: present trends and future perspectives. J Pediatr Gastroenterol Nutr 2016; 62: 521-9.
7. Choi S, Friso S. Epigenetics: a new bridge between nutrition and health. Adv Nutr 2010; 1: 8-16.
8. Barua S, Junaid M. Lifestyle, pregnancy and epigenetic effects. Epigenomics 2015; 7: 85-102.
9. Takahashi K, Sugi Y, Hosono A, et al. Epigenetic regulation of TLR4 gene expression in intestinal epithelial cells for the maintenance of intestinal homeostasis. J Immunol 2009; 183: 6522-29.
10. Koenig JE, Spor A, Scalfone N, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci 2011; 108: 4578-85.
11. Mackie RI, Sghir A, Gaskins HR. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr. 1999; 69: 1035s-45s.
12. Bach JF. The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med 2002; 347: 911-20.
13. Thorburn AN, Macia L, Mackay CR. Diet, metabolites and "Western-Lifestyle" inflammatory bowel disease. Immunity 2014; 40: 833-42.
14. Kaplan J, Shi H, Walker W. The role of microbes in developmental immunologic programming. Pediatr Res 2011; 69: 465-72.
15. Guarner F, Bourdet-Sicard R, Rook G, et al. Mechanisms of disease: the hygiene hypothesis revisited. Nat Clin Pract Gastroenterol Hepatol 2006; 3: 275.
16. Wills-Karp M, Santeliz J, Karp C. The germless theory of allergic disease: revisiting the hygiene hypothesis. Nat Rev Immunol 2001; 1: 69-75.
17. Shanahan F. The gut microbiota-a clinical perspective on lessons learned. Nat Rev Gastroenterol Hepatol 2012; 9: 609-14.
18. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med 2014; 6: 237.
19. Donnet-Hughes A, Perez PF, Doré J, et al. Potential role of the intestinal microbiota of the mother in neonatal immune education. Proc Nut Soc 2010; 69: 407-15.
20. Perez PF, Dore J, Leclerc M, et al. Bacterial imprinting of the neonatal immune system: lessons from maternal cells Pediatrics 2007; 119: e725-32.
21. Ardissone AN, de la Cruz DM, Davis-Richardson A, et al. Meconium microbiome analysis identifies bacteria correlated with preterm birth. PLoS ONE 2014; 9: e90784.
22. Karlsson M, Kahu H, Hanson L, et al. Neonatal colonization of rats induces immunological tolerance to bacterial antigens. Eur J Immunol 1999; 29: 109-18.
23. Schwartz S, Friedberg I, Ivanov IV, et al. A metagenomic study of dietdependent interaction between gut microbiota and host in infants reveals differences in immune response. Genome Biol 2012; 13: r3.
24. Chichlowski M, De Lartigue G, German JB, et al. Bifidobacteria isolated from infants and cultured on human milk oligosaccharides affect intestinal epithelial function. J Pediatr Gastroenterol Nutr 2012; 55: 321-7.
25. Sudo N, Sawamura S, Tanaka K, et al. The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction. J Immunol 1997; 159: 1739-45.
26. Olszak T, An D, Blumberg R, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 2012; 6080: 489-93.
27. Weng M, Walker WA. The role of gut microbiota in programming the immune phenotype. J Dev Origin Health Dis 2013; 4: 203-14.
28. Walker WA, Iyengar RS. Breast milk, microbiota and intestinal immune homeostasis. Pediatr Res 2015; 77: 220-8.
29. Torrow N, Hornef M. The neonatal window of opportunity: setting the stage for life-long host-microbial interaction and immune homeostasis. J Immunol 2017; 198: 557-63.
30. Jost T, Lacroix C, Braegger CP, et al. New insights in gut microbiota establishment in healthy breast fed neonates. PLoS ONE 2012; 7: e44595.
31. Furuta G, Walker WA. Non-immune defense mechanisms of the gastrointestinal tract. In: Blaser MJ, Smith PD, Ravdin JI et al., eds. Infections of the Gastrointestinal Tract. New York, NY: Raven Press Ltd, 1995: 89-98.
32. Rautava S, Walker WA. Breatfeeding-an extrauterine link between mother and child. Breastfeed Med 2009; 4: 3-10.
33. Newburg DS, Walker WA. Protection of the neonate by the immune system of developing gut and of human milk. Pediatr Res 2007; 61: 2-8.
34. Gregory KE, Walker WA. Immunologic factors in human milk and disease prevention in the preterm infant. Curr Pediatr Rep 2013; 1: 222-8.
35. Wijendran V, Brenna JT, Walker WA, et al. Long chain polyunsaturated fatty acids attenuate the IL-1induced pro-inflammatory response in human fetal intestinal epithelial cells. Pediatr Res 2015; 78: 626-33.
36. Rautava S, Nanthakumar NN, Walker WA, et al. Breast milk transforming growth factor-2 specifically attenuates IL-1-induced inflammatory responses in the immature human intestine via a SMAD6 and ERK-dependent mechanism. Neonatology 2010; 99: 192-201.
37. Yoshioka H, Iseki K, Fujita K. Development and differences of intestinal flora in the neonatal period in breast-fed and bottle-fed infants. Pediatrics 1983; 72: 317-21.
38. Jeurink P, van Bergenhenegouwen J, Martín R, et al. Human milk: a source of more life than we imagine. Benef Microbes 2013; 4: 17-30.
39. Martín R, Heilig G, Zoetendal E, et al. Diversity of the Lactobacillus group in breast milk and vagina of healthy women and potential role in the colonization of the infant gut. J Appl Microbiol 2007; 103: 2638-44.
40. Cabrera-Rubio R, Collado M, Laitinen K, et al. The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr 2012; 96: 544-1.
41. Martin CR, Walker WA. Innate and mucosal immunity in the developing GI tract: relationship to early and later disease. In: Gleason CA, Devaskar SU, eds. Avery's Diseases of the Newborn, 9th edn. St Louis, MO: Elsevier/Saunders, 2011: 994-1006.
42. Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol 2008; 8: 411-20.
43. Ganz T. Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol 2003; 3: 7190-20.
44. Johansson MEV, Larsson JMH, Hansson GC. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc Natl Acad Sci 2011; 108: 4659-65.
45. Sansonetti PJ. War and peace at mucosal surfaces. Nat Rev Immunol 2004; 4: 953-64.
46. Neutra MR. M cells in antigen sampling in mucosal tissues. Curr Top Microbial Immunol 1999; 236: 17-32.
47. Hansen CHF, Nielsen DS, Kverka M, et al. Patterns of early gut colonization shape future immune responses of the host. PLoS ONE 2012; 7: e34043.
48. Bollrath F, Powrie F. Feed your Tregs more fiber. Science 2013; 341: 463-.
49. Smith PM, Howitt MR, Panikov N, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013; 341: 569-73.
50. Mazmanian SK, Liu CH, Tzianabos AO, et al. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005; 122: 107-8.
51. Mazmanian SK, Kasper DL. The love-hate relationship between bacterial polysaccharides and the host immune system. Nat Rev Imnunol 2006; 6: 849-58.
52. Atarashi K, Tanoue T, Shima T, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011; 331: 337-41.
53. Kiss EA, Vonarbourg C, Kopfmann S, et al. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 2011; 334: 1561-5.
54. Weiner HL, da Cunha AP, Quintana F, Wu H. Oral tolerance. Immunol Rev 2011; 241: 241-59.
55. Petersson J, Schreiber O, Hansson GC, et al. Importance and regulation of the colonic mucus barrier in a mouse model of colitis. J Physiol Gastrointest Liver Physiol 2011; 300: G327-33.
56. McAuley JL, Linden SK, Png CW, et al. MUC1 cell surface mucin is a critical element of the mucosal barrier to infection. J Clin Invest 2007; 117: 2313-4.
57. Frey A, Giannasca KT, Weltzin R, et al. Role of the glycocalyx in regulating access of microparticles to apical plasma membranes of intestinal epithelial cells implications for microbial attachment and oral vaccine targeting. J Exp Med 1996; 184: 1045-59.
58. Ahern PP, Faith JJ, Gordon JI. Mining the human gut microbiota for effector strains that shape the immune system. Immunity 2014; 40: 815-23.
59. Walker WA. Dysbiosis: In: Floch MH, Ringel Y, Walker WA, eds. The Microbiota in Gastrointestinal Pathophysiology: Implications for Human Health, Prebiotics, Probiotics and Dysbiosis, Ch 25. Elsevier Inc: New York, USA, 2016: 227-231.
60. Jakobsson HE, Abrahamsson TR, Jenmalm MC, et al. Decreased gut microbiota diversity, delayed bacteroides colonization and reduced Th1 responses in infants delivered by caesarean section. Gut 2013; 63: 559-66.
61. Chu D, Ma J, Prince A, et al. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat Med 2017; 1: 1-15.
62. Sevelsted A, Stokholm J, Bønnelykke K, et al. Cesarean section and chronic immune disorders. Pediatrics 2015; 135: e92-8.
63. Mårild K, Stephansson O, Montgomery S, et al. Pregnancy outcome and risk of celiac disease in offspring: a nationwide case-control study. Gastroenterology 2012; 142: 39-45.
64. Decker E, Engelmann G, Findeisen A, et al. Cesarean delivery is associated with celiac disease but not inflammatory bowel disease in children. Pediatrics 2010; 125: e1433-40.
65. Mesquita DN, Barbieri MA, Goldani HA, et al. Cesarean section is associated with increased peripheral and central adiposity in young adulthood: cohort study. PLoS ONE 2013; 8: e66827.
66. Thavagnanam S, Fleming J, Bromley A, et al. A meta-analysis of the association between Caesarean section and childhood asthma. Clin Exp Allergy 2008; 38: 629-33.
67. Chu D, Ma J, Prince A, et al. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat Med 2017; 23: 314-26.
68. Penders J, Stobberingh EE, van den Brandt, et al. The role of the intestinal microbiota in the development of atopic disorders. Allergy 2007; 62: 1223-36.
69. Zeissig S, Blumberg RS. Life at the beginning: perturbation of the microbiota by antibiotics in early life and its role in health and disease. Nature Immunol 2014; 12: 307-10.
70. An D, Oh SF, Olszak T, et al. Sphingolipids from a symbiotic microbe regulate homeostasis of host intestinal natural killer T cells. Cell 201: 123-33.
71. Marra F, Marra CA, Richardson K, et al. Antibiotic use in children is associated with increased risk of asthma. Pediatrics 2009; 123: 1003-10.
72. Giongo A, Gano KA, Drabb DB, et al. Toward defining the autoimmune microbiome for type 1 diabetes. ISME J 2011; 5: 82-91.
73. Trasande L, Blustein J, Liu M, et al. Infant antibiotic exposures and early-life body mass. Int J Obes 2013; 37: 16-23.
74. Zhou Y, Shan G, Sodergren E, et al. Longitudinal analysis of preterm intestinal microbiome prior to necrotizing enterocolitis: a case-control study. PLoS ONE 2015; 10: e0118632.
75. Nanthakumar N, Meng D, Goldstein AM, et al. The mechanism of excessive intestinal inflammation in necrotizing enterocolitis: An immature innate immune response. PLoS ONE 2011; 6: e17776.
76. Gregory KE, Samuel BS, Houghteling P, et al. Influence of maternal breast milk ingestion on acquisition of the intestinal microbiome in preterm infants. Microbiome 2016; 4: 68.
77. Million M, Lagier J-C, Yahav D, Paul M. Gut bacterial microbiota and obesity. Clin Microbiol Infect 2013; 19: 305-13.
78. Galley JD, Bailey M, Dush CK, Schoppe-Sullivan S, Christian LM. Maternal obesity is associated with alterations in the gut microbiome in toddlers. PLoS ONE 2014; 9: e-112026.
79. Baker JL, Michalesen KF, Rasmussen KM, Sorensen TIA. Maternal prepregnant body mass index, duration of breastfeeding, and timing of complementary food introduction are associated with infant weight gain. Am J Clin Nutr 2004; 80: 1579-88.
80. McFarland L. Use of probiotics to correct dysbiosis of normal microbiota following disease or disruptive events: a systematic review. BMJ Open 2014; 4: 1.
81. Belizário J, Napolitano M. Human microbiomes and their roles in dysbiosis, common diseases, and novel therapeutic approaches. Front Microbiol 2015; 6: 1050.
82. Petersen C, Round J. Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol 2014; 16: 1024-33.
83. De Filippo C, Cavalieri D, Di Paola M, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci 2010; 107: 14691-6.
84. Wu GD, Chen J, Hoffmann C, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011; 334: 105-8.
85. Faith JJ, Guruge JL, Charbonneau M, et al. The long-term stability of the human gut microbiota. Science 2013; 341: 1237439.
86. Chassaing B, Koren O, Godrich JK, et al. Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature 2015; 519: 92-6.
87. Zenhom M, Hyder A, de Vrese M, et al. Prebiotic oligosaccharides reduce proinflammatory cytokines in intestinal Caco-2 cells via activation of PPAR and preptidoglycan recognition protein 3. J Nutr 2011; 141: 971-7.
88. Bakker-Zieikzee AM, van Tol EAF, Kroes H, Alles MS, Kok FJ, Bindels JD. Fecal SIgA secretion in infants fed on pre-or probiotic infant formula. Pediatr Allergy Immunol 2006; 17: 134-40.
89. Chichlowski M, DeLartigue G, German JB, Raybould HE, Mills DA. Bifidobacteria isolated from infants and cultured on human milk oligosaccharides affect intestinal epithelial function. J Pediatr Gastro Nutr 2012; 55: 321-7.
90. Newburg DS, Ko JS, Leone S, Nanthakumar NN. Human milk oligosaccharides and synthetic galactosyloligosaccharides contain 3-, 4-4, and 6-galactosyllactose and attenuate inflammation in human T84, NCM-460, and H4 cells and intestinal tissue ex vivo. J Nutr 2016; 146: 358-67.
91. Ten Bruggencate SJM, Bovee-Oudenhoven IMJ, Letink-Wissink MLG, Kata MB, ven der Merr R. Dietary fructooligosaccarides affect intestinal barrier function in healthy men. J Nutr 2006; 136: 70-4.
92. Moro G, Arslanoglu S, Stahl B, Jelinek J, Wahn U, Boehm G. A mixture of prebiotic oligosaccharides reduces the incident of atopic dermatitis during the first six months of age. Arch Dis Child 2006; 91: 814-19.
93. Lindsay JO, Whelan K, Stagg AJ, et al. The clinical, microbiological and immunological effects of fructo-oligosaccharide in patients with Crohn's disease. Gut 2006; 55: 348-55.
94. Gruber C, van Stujvengerg M, Mosca F, et al. Reduced occurrence of early atopic dermatitis because of immunoactive prebiotics among lowatopy-risk infants. J Allergy Clin Immunol 2010; 126: 791-7.
95. Boehm G, Jelinek J, Stahl B, et al. Prebiotics in infant formulas. J Clin Gastroenterol 2004; 38: S76-9.
96. Silk DB, Davis A, Vulevic J, Tzortzis G, Gibson GR. Clinical trial: The effects of a trans-galactooligosaccharide prebiotic on faecal microbiota and symptoms in irritable bowel syndrome. Aliment Pharmacol Ther 2009; 29: 508-18.
97. Xia Q, Williams T, Hustead D, Price P, Morrison M, Yu Z. Quantitative analysis of intestinal bacterial populations from term infants fed formula supplemented with fructo-oligosaccharides. J Pediatr Gastroenterol Nutr 2013; 55: 314-20.
98. Gareau MG, Sherman PM, Walker WA. Probiotics and the gut microbiota in intestinal health and disease. Nature Rev: Gastroenterol Hepatol 2010; 7: 503-14.
99. Kamada N, Chen G, Nunez G. Harnessing pathogen-commensal relations. Nature Med 2012; 18: 1190-1.
100. Mack DR, Michael S, Wei S, McDougall L, Hollingsworth MA. Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am J Physiol Gastrointest Liver Physiol 1999; 39: G941-50.
101. Thomas DW, Greer FR, et al. Clinical report-probiotics and prebiotics in pediatrics. Pediatrics 2010; 126: 1217-31.
102. Smits LP, Bouter KEC, de Vos WM, Borody T, Nieuwdorp M. Therapeutic potential of fecal microbiota transplantation. Gastroenterology 2013; 145: 946-53.
103. Dutta SK, Girota M, Garg S, et al. Efficacy of combined jejuna and colonic fecal microbiota transplantation for recurrent clostridium difficile infection. Clin Gastroenterol Hepatol 2014; 12: 1572-6.
104. Hourigan SK, Oliva-Hemker M. Fecal microbiota transplantation in children: a brief review. Pediatr Res 2016; 80: 2-6.
105. Knaapen M, Kootte RS, Zoetendal EG, et al. Obesity, non-alcoholic fatty liver disease and atherothrombosis: a role for the intestinal microbiota Clin Microbiol Infect 2013; 19: 331-7.