Early development of the gut microbiota and immune health

Pathogens

Volumn 3, Issue 3, 2014, Pages 769-790

  Francino, M Pilar ^a,b  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Antibiotics; Atopy; Early programming; Gut microbiota; Human microbiome; Immune disease; Infant gut; Intrauterine transmission; Microbe host interactions; Necrotizing enterocolitis

Indexed keywords

CD14 ANTIGEN; FLAGELLIN; INTERLEUKIN 10; LIPOPOLYSACCHARIDE; MUCIN 2; MURAMIC ACID; PEPTIDOGLYCAN; POLYSACCHARIDE; PREBIOTIC AGENT; PROBIOTIC AGENT; SHORT CHAIN FATTY ACID; TRANSFORMING GROWTH FACTOR BETA;

ACTINOBACTERIA; ARTIFICIAL MILK; ATOPY; AUTOIMMUNE DISEASE; BACTERIAL TRANSMISSION; BACTEROIDES; BIFIDOBACTERIUM; BREAST FEEDING; BREAST MILK; CESAREAN SECTION; CLOSTRIDIUM; CORYNEBACTERIUM; DISEASE ASSOCIATION; ENTEROCOCCUS; ENTEROCOCCUS FAECIUM; ESCHERICHIA; FAECALIBACTERIUM; HELPER CELL; HUMAN; HUMAN DEVELOPMENT; IMMUNE SYSTEM; IMMUNITY; IMMUNOPATHOLOGY; INFANCY; INTESTINE FLORA; LACTOBACILLUS; LACTOCOCCUS; META ANALYSIS (TOPIC); MICROBIAL COLONIZATION; NECROTIZING ENTEROCOLITIS; NONHUMAN; ORGANISMAL INTERACTION; PREMATURE LABOR; PREVOTELLA; PROPIONIBACTERIUM; PYROSEQUENCING; RANDOMIZED CONTROLLED TRIAL (TOPIC); REGULATORY T LYMPHOCYTE; REVIEW; RUMINOCOCCUS; STAPHYLOCOCCUS; SYSTEMATIC REVIEW (TOPIC); WEISSELLA;

EID: 85000634220     PISSN: None     EISSN: 20760817     Source Type: Journal    
DOI: 10.3390/pathogens3030769     Document Type: Review

References (171)

1. Lewis, J.F.; Johnson, P.; Miller, P. Evaluation of amniotic fluid for aerobic and anaerobic bacteria. Am. J. Clin. Pathol. 1976, 65, 58-63.
2. Gibbs, R.S.; Blanco, J.D.; St Clair, P.J.; Castaneda, Y.S. Quantitative bacteriology of amniotic fluid from women with clinical intraamniotic infection at term. J. Infect. Dis. 1982, 145, 1-8.
3. Dong, Y.; St Clair, P.J.; Ramzy, I.; Kagan-Hallet, K.S.; Gibbs, R.S. A microbiologic and clinical study of placental inflammation at term. Obstet. Gynecol. 1987, 70, 175-182.
4. Romero, R.; Sirtori, M.; Oyarzun, E.; Avila, C.; Mazor, M.; Callahan, R.; Sabo, V.; Athanassiadis, A.P.; Hobbins, J.C. Infection and labor. V. Prevalence, microbiology, and clinical significance of intraamniotic infection in women with preterm labor and intact membranes. Am. J. Obstet. Gynecol. 1989, 161, 817-824.
5. Romero, R.; Mazor, M.; Morrotti, R.; Avila, C.; Oyarzun, E.; Insunza, A.; Parra, M.; Behnke, E.; Montiel, F.; Cassell, G.H. Infection and labor. VII. Microbial invasion of the amniotic cavity in spontaneous rupture of membranes at term. Am. J. Obstet. Gynecol. 1992, 166 (1 Pt 1), 129-133.
6. DiGiulio, D.B.; Romero, R.; Amogan, H.P.; Kusanovic, J.P.; Bik, E.M.; Gotsch, F.; Kim, C.J.; Erez, O.; Edwin, S.; Relman, D.A. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: A molecular and culture-based investigation. PLoS One 2008, 3, e3056.
7. DiGiulio, D.B.; Romero, R.; Kusanovic, J.P.; Gomez, R.; Kim, C.J.; Seok, K.S.; Gotsch, F.; Mazaki-Tovi, S.; Vaisbuch, E.; Sanders, K. et al. Prevalence and diversity of microbes in the amniotic fluid, the fetal inflammatory response, and pregnancy outcome in women with preterm pre-labor rupture of membranes. Am. J. Reprod. Immunol. 2010, 64, 38-57.
8. Jimenez, E.; Fernandez, L.; Marin, M.L.; Martin, R.; Odriozola, J.M.; Nueno-Palop, C.; Narbad, A.; Olivares, M.; Xaus, J.; Rodriguez, J.M. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr. Microbiol. 2005, 51, 270-274.
9. Roos, P.J.; Malan, A.F.; Woods, D.L.; Botha, P.; Hyland, J.; Heese Hde, V. The bacteriological environment of preterm infants. S. Afr. Med. J. 1980, 57, 347-350.
10. Jimenez, E.; Marin, M.L.; Martin, R.; Odriozola, J.M.; Olivares, M.; Xaus, J.; Fernandez, L.; Rodriguez, J.M. Is meconium from healthy newborns actually sterile? Res. Microbiol. 2008, 159, 187-193.
11. Moles, L.; Gomez, M.; Heilig, H.; Bustos, G.; Fuentes, S.; de Vos, W.; Fernandez, L.; Rodriguez, J.M.; Jimenez, E. Bacterial diversity in meconium of preterm neonates and evolution of their fecal microbiota during the first month of life. PLoS One 2013, 8, e66986.
12. Perez, P.F.; Dore, J.; Leclerc, M.; Levenez, F.; Benyacoub, J.; Serrant, P.; Segura-Roggero, I.; Schiffrin, E.J.; Donnet-Hughes, A. Bacterial imprinting of the neonatal immune system: Lessons from maternal cells? Pediatrics 2007, 119, e724-e732.
13. Dominguez-Bello, M.G.; Costello, E.K.; Contreras, M.; Magris, M.; Hidalgo, G.; Fierer, N.; Knight, R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. USA 2010, 107, 11971-11975.
14. Mshvildadze, M.; Neu, J.; Shuster, J.; Theriaque, D.; Li, N.; Mai, V. Intestinal microbial ecology in premature infants assessed with non-culture-based techniques. J. Pediatr. 2010, 156, 20-25.
15. Madan, J.C.; Salari, R.C.; Saxena, D.; Davidson, L.; O’Toole, G.A.; Moore, J.H.; Sogin, M.L.; Foster, J.A.; Edwards, W.H.; Palumbo, P. et al. Gut microbial colonisation in premature neonates predicts neonatal sepsis. Arch. Dis. Child. Fetal Neonatal Ed. 2012, 97, F456-F462.
16. Gosalbes, M.J.; Llop, S.; Valles, Y.; Moya, A.; Ballester, F.; Francino, M.P. Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clin. Exp. Allergy 2013, 43, 198-211.
17. Hu, J.; Nomura, Y.; Bashir, A.; Fernandez-Hernandez, H.; Itzkowitz, S.; Pei, Z.; Stone, J.; Loudon, H.; Peter, I. Diversified microbiota of meconium is affected by maternal diabetes status. PLoS One 2013, 8, e78257.
18. Vallès, Y.; Gosalbes, M.J.; de Vries, L.E.; Abellan, J.J.; Francino, M.P. Metagenomics and development of the gut microbiota in infants. Clin. Microbiol. Infect. 2012, 18 Suppl 4, 21-26.
19. Vallès, Y.; Artacho, A.; Pascual-García, A.; Ferrús, M.L.; Gosalbes, M.J.; Abellán, J.J.; Francino, M.P. Microbial Succession in the Gut: Directional Trends of Taxonomic and Functional Change in a Birth Cohort of Spanish Infants. PLoS Genetics 2014, 10, e1004406.
20. Palmer, C.; Bik, E.M.; DiGiulio, D.B.; Relman, D.A.; Brown, P.O. Development of the human infant intestinal microbiota. PLoS Biol. 2007, 5, e177.
21. Yatsunenko, T.; Rey, F.E.; Manary, M.J.; Trehan, I.; Dominguez-Bello, M.G.; Contreras, M.; Magris, M.; Hidalgo, G.; Baldassano, R.N.; Anokhin, A.P. et al. Human gut microbiome viewed across age and geography. Nature 2012, 486, 222-227.
22. Vaishampayan, P.A.; Kuehl, J.V.; Froula, J.L.; Morgan, J.L.; Ochman, H.; Francino, M.P. Comparative metagenomics and population dynamics of the gut microbiota in mother and infant. Genome Biol. Evol. 2010, 2, 53-66.
23. Kurokawa, K.; Itoh, T.; Kuwahara, T.; Oshima, K.; Toh, H.; Toyoda, A.; Takami, H.; Morita, H.; Sharma, V.K.; Srivastava, T.P. et al. Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res.: Int. J. Rapid Publ. Rep. Genes Genomes 2007, 14, 169-181.
24. Koenig, J.E.; Spor, A.; Scalfone, N.; Fricker, A.D.; Stombaugh, J.; Knight, R.; Angenent, L.T.; Ley, R.E. Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. USA 2011, 108 Suppl 1, 4578-4585.
25. Wold, A.E. The hygiene hypothesis revised: Is the rising frequency of allergy due to changes in the intestinal flora? Allergy 1998, 53 (46 Suppl), 20-25.
26. Bjorksten, B. Environment and infant immunity. Proc. Nutr. Soc. 1999, 58, 729-732.
27. Noverr, M.C.; Huffnagle, G.B. The ‘microflora hypothesis’ of allergic diseases. Clin. Exp. Allergy 2005, 35, 1511-1520.
28. Strachan, D.P. Hay fever, hygiene, and household size. BMJ 1989, 299, 1259-1260.
29. Von Mutius, E.; Martinez, F.D.; Fritzsch, C.; Nicolai, T.; Reitmeir, P.; Thiemann, H.H. Skin test reactivity and number of siblings. BMJ 1994, 308, 692-695.
30. Ball, T.M.; Castro-Rodriguez, J.A.; Griffith, K.A.; Holberg, C.J.; Martinez, F.D.; Wright, A.L. Siblings, day-care attendance, and the risk of asthma and wheezing during childhood. N. Engl. J. Med. 2000, 343, 538-543.
31. Benn, C.S.; Melbye, M.; Wohlfahrt, J.; Bjorksten, B.; Aaby, P. Cohort study of sibling effect, infectious diseases, and risk of atopic dermatitis during first 18 months of life. BMJ 2004, 328, 1223.
32. Bjorksten, B.; Naaber, P.; Sepp, E.; Mikelsaar, M. The intestinal microflora in allergic Estonian and Swedish 2-year-old children. Clin. Exp. Allergy 1999, 29, 342-346.
33. Bjorksten, B.; Sepp, E.; Julge, K.; Voor, T.; Mikelsaar, M. Allergy development and the intestinal microflora during the first year of life. J. Allergy Clin. Immunol. 2001, 108, 516-520.
34. Kalliomaki, M.; Kirjavainen, P.; Eerola, E.; Kero, P.; Salminen, S.; Isolauri, E. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J. Allergy Clin. Immunol. 2001, 107, 129-134.
35. Penders, J.; Stobberingh, E.E.; Thijs, C.; Adams, H.; Vink, C.; van Ree, R.; van den Brandt, P.A. Molecular fingerprinting of the intestinal microbiota of infants in whom atopic eczema was or was not developing. Clin. Exp. Allergy 2006, 36, 1602-1608.
36. Penders, J.; Thijs, C.; van den Brandt, P.A.; Kummeling, I.; Snijders, B.; Stelma, F.; Adams, H.; van Ree, R.; Stobberingh, E.E. Gut microbiota composition and development of atopic manifestations in infancy: The KOALA Birth Cohort Study. Gut 2007, 56, 661-667.
37. Wang, M.; Karlsson, C.; Olsson, C.; Adlerberth, I.; Wold, A.E.; Strachan, D.P.; Martricardi, P.M.; Aberg, N.; Perkin, M.R.; Tripodi, S. et al. Reduced diversity in the early fecal microbiota of infants with atopic eczema. J. Allergy Clin. Immunol. 2008, 121, 129-134.
38. Sjogren, Y.M.; Jenmalm, M.C.; Bottcher, M.F.; Bjorksten, B.; Sverremark-Ekstrom, E. Altered early infant gut microbiota in children developing allergy up to 5 years of age. Clin. Exp. Allergy 2009, 39, 518-526.
39. Bisgaard, H.; Li, N.; Bonnelykke, K.; Chawes, B.L.; Skov, T.; Paludan-Muller, G.; Stokholm, J.; Smith, B.; Krogfelt, K.A. Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J. Allergy Clin. Immunol. 2011, 128, 646-652.e1-5.
40. Abrahamsson, T.R.; Jakobsson, H.E.; Andersson, A.F.; Bjorksten, B.; Engstrand, L.; Jenmalm, M.C. Low diversity of the gut microbiota in infants with atopic eczema. J. Allergy Clin. Immunol. 2012, 129, 434-440, 440 e1-2.
41. Kuvaeva, I.B.; Orlova, N.G.; Veselova, O.L.; Kuznezova, G.G.; Borovik, T.E. Microecology of the gastrointestinal tract and the immunological status under food allergy. Nahrung 1984, 28, 689-693.
42. Sepp, E.; Julge, K.; Vasar, M.; Naaber, P.; Bjorksten, B.; Mikelsaar, M. Intestinal microflora of Estonian and Swedish infants. Acta Paediatr. 1997, 86, 956-961.
43. Sepp, E.; Julge, K.; Mikelsaar, M.; Bjorksten, B. Intestinal microbiota and immunoglobulin E responses in 5-year-old Estonian children. Clin. Exp. Allergy 2005, 35, 1141-1146.
44. Mah, K.W.; Bjorksten, B.; Lee, B.W.; van Bever, H.P.; Shek, L.P.; Tan, T.N.; Lee, Y.K.; Chua, K.Y. Distinct pattern of commensal gut microbiota in toddlers with eczema. Int Arch. Allergy Immunol. 2006, 140, 157-163.
45. Murray, C.S.; Tannock, G.W.; Simon, M.A.; Harmsen, H.J.; Welling, G.W.; Custovic, A.; Woodcock, A. Fecal microbiota in sensitized wheezy and non-sensitized non-wheezy children: A nested case-control study. Clin. Exp. Allergy 2005, 35, 741-745.
46. Ouwehand, A.C.; Isolauri, E.; He, F.; Hashimoto, H.; Benno, Y.; Salminen, S. Differences in Bifidobacterium flora composition in allergic and healthy infants. J. Allergy Clin. Immunol. 2001, 108, 144-145.
47. He, F.; Ouwehand, A.C.; Isolauri, E.; Hosoda, M.; Benno, Y.; Salminen, S. Differences in composition and mucosal adhesion of bifidobacteria isolated from healthy adults and healthy seniors. Curr. Microbiol. 2001, 43, 351-354.
48. Smits, H.H.; Hartgers, F.C.; Yazdanbakhsh, M. Helminth infections: Protection from atopic disorders. Curr. Allergy Asthma Rep. 2005, 5, 42-50.
49. Von der Weid, T.; Bulliard, C.; Schiffrin, E.J. Induction by a lactic acid bacterium of a population of CD4(+) T cells with low proliferative capacity that produce transforming growth factor beta and interleukin-10. Clin. Diagn. Lab. Immunol. 2001, 8, 695-701.
50. Christensen, H.R.; Frokiaer, H.; Pestka, J.J. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J. Immunol. 2002, 168, 171-178.
51. Rook, G.A.; Adams, V.; Hunt, J.; Palmer, R.; Martinelli, R.; Brunet, L.R. Mycobacteria and other environmental organisms as immunomodulators for immunoregulatory disorders. Springer Semin. Immunopathol. 2004, 25, 237-255.
52. Mohamadzadeh, M.; Olson, S.; Kalina, W.V.; Ruthel, G.; Demmin, G.L.; Warfield, K.L.; Bavari, S.; Klaenhammer, T.R. Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Proc. Natl. Acad. Sci. USA 2005, 102, 2880-2885.
53. Penders, J.; Stobberingh, E.E.; van den Brandt, P.A.; Thijs, C. The role of the intestinal microbiota in the development of atopic disorders. Allergy 2007, 62, 1223-1236.
54. Bottcher, M.F.; Nordin, E.K.; Sandin, A.; Midtvedt, T.; Bjorksten, B. Microflora-associated characteristics in faeces from allergic and nonallergic infants. Clin. Exp. Allergy 2000, 30, 1590-1596.
55. Linneberg, A.; Ostergaard, C.; Tvede, M.; Andersen, L.P.; Nielsen, N.H.; Madsen, F.; Frolund, L.; Dirksen, A.; Jorgensen, T. IgG antibodies against microorganisms and atopic disease in Danish adults: The Copenhagen Allergy Study. J. Allergy Clin. Immunol. 2003, 111, 847-853.
56. Woolcock, A.J.; Peat, J.K. Evidence for the increase in asthma worldwide. Ciba Found. Symp. 1997, 206, 122-134; discussion 134-139, 157-159.
57. Thompson-Chagoyan, O.C.; Fallani, M.; Maldonado, J.; Vieites, J.M.; Khanna, S.; Edwards, C.; Dore, J.; Gil, A. Faecal microbiota and short-chain fatty acid levels in faeces from infants with cow’s milk protein allergy. Int. Arch. Allergy Immunol. 2011, 156, 325-332.
58. Sandin, A.; Braback, L.; Norin, E.; Bjorksten, B. Faecal short chain fatty acid pattern and allergy in early childhood. Acta Paediatr. 2009, 98, 823-827.
59. Schulzke, S.M.; Deshpande, G.C.; Patole, S.K. Neurodevelopmental outcomes of very low-birth-weight infants with necrotizing enterocolitis: A systematic review of observational studies. Arch. Pediatr. Adolesc. Med. 2007, 161, 583-590.
60. Mai, V.; Young, C.M.; Ukhanova, M.; Wang, X.; Sun, Y.; Casella, G.; Theriaque, D.; Li, N.; Sharma, R.; Hudak, M. et al. Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLoS One 2011, 6, e20647.
61. Mai, V.; Torrazza, R.M.; Ukhanova, M.; Wang, X.; Sun, Y.; Li, N.; Shuster, J.; Sharma, R.; Hudak, M.L.; Neu, J. Distortions in development of intestinal microbiota associated with late onset sepsis in preterm infants. PLoS One 2013, 8, e52876.
62. Platt, A.M.; Mowat, A.M. Mucosal macrophages and the regulation of immune responses in the intestine. Immunol. Lett. 2008, 119, 22-31.
63. Romagnani, S. Regulation of the T cell response. Clin. Exp. Allergy 2006, 36, 1357-1366.
64. Groux, H.; O’Garra, A.; Bigler, M.; Rouleau, M.; Antonenko, S.; de Vries, J.E.; Roncarolo, M.G. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997, 389, 737-742.
65. Romagnani, S. The increased prevalence of allergy and the hygiene hypothesis: Missing immune deviation, reduced immune suppression, or both? Immunology 2004, 112, 352-363.
66. Akdis, M. Healthy immune response to allergens: T regulatory cells and more. Curr. Opin. Immunol. 2006, 18, 738-744.
67. Meiler, F.; Klunker, S.; Zimmermann, M.; Akdis, C.A.; Akdis, M. Distinct regulation of IgE, IgG4 and IgA by T regulatory cells and toll-like receptors. Allergy 2008, 63, 1455-1463.
68. Mosmann, T.R.; Cherwinski, H.; Bond, M.W.; Giedlin, M.A.; Coffman, R.L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 1986, 136, 2348-2357.
69. Parronchi, P.; de Carli, M.; Manetti, R.; Simonelli, C.; Sampognaro, S.; Piccinni, M.P.; Macchia, D.; Maggi, E.; Del Prete, G.; Romagnani, S. IL-4 and IFN (alpha and gamma) exert opposite regulatory effects on the development of cytolytic potential by Th1 or Th2 human T cell clones. J. Immunol. 1992, 149, 2977-2983.
70. Gajewski, T.F.; Fitch, F.W. Anti-proliferative effect of IFN-gamma in immune regulation. I. IFN-gamma inhibits the proliferation of Th2 but not Th1 murine helper T lymphocyte clones. J. Immunol. 1988, 140, 4245-4252.
71. Oboki, K.; Ohno, T.; Saito, H.; Nakae, S. Th17 and allergy. Allergol Int. 2008, 57, 121-134.
72. Abbas, A.K. Die and let live: Eliminating dangerous lymphocytes. Cell 1996, 84, 655-657.
73. Murphy, K.M. In search of the CTD. Nat. Immunol. 2003, 4, 645.
74. Nakae, S.; Komiyama, Y.; Nambu, A.; Sudo, K.; Iwase, M.; Homma, I.; Sekikawa, K.; Asano, M.; Iwakura, Y. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 2002, 17, 375-387.
75. Akdis, C.A.; Akdis, M. Mechanisms and treatment of allergic disease in the big picture of regulatory T cells. J. Allergy Clin. Immunol. 2009, 123, 735-746.
76. Rook, G.A.; Brunet, L.R. Microbes, immunoregulation, and the gut. Gut 2005, 54, 317-320.
77. Rautava, S.; Ruuskanen, O.; Ouwehand, A.; Salminen, S.; Isolauri, E. The hygiene hypothesis of atopic disease--an extended version. J. Pediatr. Gastroenterol. Nutr. 2004, 38, 378-388.
78. Yazdanbakhsh, M.; Kremsner, P.G.; van Ree, R. Allergy, parasites, and the hygiene hypothesis. Science 2002, 296, 490-494.
79. Wills-Karp, M.; Santeliz, J.; Karp, C.L. The germless theory of allergic disease: Revisiting the hygiene hypothesis. Nat. Rev. Immunol. 2001, 1, 69-75.
80. Strauch, U.G.; Obermeier, F.; Grunwald, N.; Gurster, S.; Dunger, N.; Schultz, M.; Griese, D.P.; Mahler, M.; Scholmerich, J.; Rath, H.C. Influence of intestinal bacteria on induction of regulatory T cells: Lessons from a transfer model of colitis. Gut 2005, 54, 1546-1552.
81. Kline, J.N. Eat dirt: CpG DNA and immunomodulation of asthma. Proc. Am. Thorac. Soc. 2007, 4, 283-288.
82. Baba, N.; Samson, S.; Bourdet-Sicard, R.; Rubio, M.; Sarfati, M. Commensal bacteria trigger a full dendritic cell maturation program that promotes the expansion of non-Tr1 suppressor T cells. J. Leukoc. Biol. 2008, 84, 468-476.
83. Ivanov, I.I.; Atarashi, K.; Manel, N.; Brodie, E.L.; Shima, T.; Karaoz, U.; Wei, D.; Goldfarb, K.C.; Santee, C.A.; Lynch, S.V. et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009, 139, 485-498.
84. Cerutti, A.; Rescigno, M. The biology of intestinal immunoglobulin A responses. Immunity 2008, 28, 740-750.
85. Bedford Russell, A.R.; Murch, S.H. Could peripartum antibiotics have delayed health consequences for the infant? BJOG 2006, 113, 758-765.
86. Tanaka, S.; Kobayashi, T.; Songjinda, P.; Tateyama, A.; Tsubouchi, M.; Kiyohara, C.; Shirakawa, T.; Sonomoto, K.; Nakayama, J. Influence of antibiotic exposure in the early postnatal period on the development of intestinal microbiota. FEMS Immunol. Med. Microbiol. 2009, 56, 80-87.
87. Fouhy, F.; Guinane, C.M.; Hussey, S.; Wall, R.; Ryan, C.A.; Dempsey, E.M.; Murphy, B.; Ross, R.P.; Fitzgerald, G.F.; Stanton, C.; Cotter, P.D. High-throughput sequencing reveals the incomplete, short-term recovery of infant gut microbiota following parenteral antibiotic treatment with ampicillin and gentamicin. Antimicrob Agents Chemother. 2012, 56, 5811-5820.
88. Deshpande, G.; Rao, S.; Patole, S.; Bulsara, M. Updated meta-analysis of probiotics for preventing necrotizing enterocolitis in preterm neonates. Pediatrics 2010, 125, 921-930.
89. Kenyon, S.L.; Taylor, D.J.; Tarnow-Mordi, W. Broad-spectrum antibiotics for preterm, prelabour rupture of fetal membranes: The ORACLE I randomised trial. ORACLE Collaborative Group. Lancet 2001, 357, 979-988.
90. Hildebrand, H.; Malmborg, P.; Askling, J.; Ekbom, A.; Montgomery, S.M. Early-life exposures associated with antibiotic use and risk of subsequent Crohn’s disease. Scand. J. Gastroenterol. 2008, 43, 961-966.
91. Kuo, C.H.; Kuo, H.F.; Huang, C.H.; Yang, S.N.; Lee, M.S.; Hung, C.H. Early life exposure to antibiotics and the risk of childhood allergic diseases: An update from the perspective of the hygiene hypothesis. J. Microbiol. Immunol. Infect. 2013, 46, 320-329.
92. Alm, J.S.; Swartz, J.; Lilja, G.; Scheynius, A.; Pershagen, G. Atopy in children of families with an anthroposophic lifestyle. Lancet 1999, 353, 1485-1488.
93. Von Mutius, E.; Illi, S.; Hirsch, T.; Leupold, W.; Keil, U.; Weiland, S.K. Frequency of infections and risk of asthma, atopy and airway hyperresponsiveness in children. Eur. Respir. J. 1999, 14, 4-11.
94. Wickens, K.L.; Crane, J.; Kemp, T.J.; Lewis, S.J.; D’Souza, W.J.; Sawyer, G.M.; Stone, M.L.; Tohill, S.J.; Kennedy, J.C.; Slater, T.M. et al. Family size, infections, and asthma prevalence in New Zealand children. Epidemiology 1999, 10, 699-705.
95. Droste, J.H.; Wieringa, M.H.; Weyler, J.J.; Nelen, V.J.; Vermeire, P.A.; van Bever, H.P. Does the use of antibiotics in early childhood increase the risk of asthma and allergic disease? Clin. Exp. Allergy 2000, 30, 1547-1553.
96. Wjst, M.; Hoelscher, B.; Frye, C.; Wichmann, H.E.; Dold, S.; Heinrich, J. Early antibiotic treatment and later asthma. Eur. J. Med. Res. 2001, 6, 263-271.
97. Thomas, M.; Custovic, A.; Woodcock, A.; Morris, J.; Simpson, A.; Murray, C.S. Atopic wheezing and early life antibiotic exposure: A nested case-control study. Pediatr. Allergy Immunol. 2006, 17, 184-188.
98. Foliaki, S.; Pearce, N.; Bjorksten, B.; Mallol, J.; Montefort, S.; von Mutius, E. Antibiotic use in infancy and symptoms of asthma, rhinoconjunctivitis, and eczema in children 6 and 7 years old: International Study of Asthma and Allergies in Childhood Phase III. J. Allergy Clin. Immunol. 2009, 124, 982-989.
99. Illi, S.; von Mutius, E.; Lau, S.; Bergmann, R.; Niggemann, B.; Sommerfeld, C.; Wahn, U. Early childhood infectious diseases and the development of asthma up to school age: A birth cohort study. BMJ 2001, 322, 390-395.
100. Celedon, J.C.; Litonjua, A.A.; Ryan, L.; Weiss, S.T.; Gold, D.R. Lack of association between antibiotic use in the first year of life and asthma, allergic rhinitis, or eczema at age 5 years. Am. J. Respir. Crit. Care Med. 2002, 166, 72-75.
101. Celedon, J.C.; Fuhlbrigge, A.; Rifas-Shiman, S.; Weiss, S.T.; Finkelstein, J.A. Antibiotic use in the first year of life and asthma in early childhood. Clin. Exp. Allergy 2004, 34, 1011-1016.
102. Harris, J.M.; Mills, P.; White, C.; Moffat, S.; Newman Taylor, A.J.; Cullinan, P. Recorded infections and antibiotics in early life: Associations with allergy in UK children and their parents. Thorax 2007, 62, 631-637.
103. Wickens, K.; Ingham, T.; Epton, M.; Pattemore, P.; Town, I.; Fishwick, D.; Crane, J. The association of early life exposure to antibiotics and the development of asthma, eczema and atopy in a birth cohort: Confounding or causality? Clin. Exp. Allergy 2008, 38, 1318-1324.
104. Mai, X.M.; Kull, I.; Wickman, M.; Bergstrom, A. Antibiotic use in early life and development of allergic diseases: Respiratory infection as the explanation. Clin. Exp. Allergy 2010, 40, 1230-1237.
105. Su, Y.; Rothers, J.; Stern, D.A.; Halonen, M.; Wright, A.L. Relation of early antibiotic use to childhood asthma: Confounding by indication? Clin. Exp. Allergy 2010, 40, 1222-1229.
106. McKeever, T.M.; Lewis, S.A.; Smith, C.; Collins, J.; Heatlie, H.; Frischer, M.; Hubbard, R. Early exposure to infections and antibiotics and the incidence of allergic disease: A birth cohort study with the West Midlands General Practice Research Database. J. Allergy Clin. Immunol. 2002, 109, 43-50.
107. Kozyrskyj, A.L.; Ernst, P.; Becker, A.B. Increased risk of childhood asthma from antibiotic use in early life. Chest 2007, 131, 1753-1759.
108. Marra, F.; Marra, C.A.; Richardson, K.; Lynd, L.D.; Kozyrskyj, A.; Patrick, D.M.; Bowie, W.R.; Fitzgerald, J.M. Antibiotic use in children is associated with increased risk of asthma. Pediatrics 2009, 123, 1003-1010.
109. Risnes, K.R.; Belanger, K.; Murk, W.; Bracken, M.B. Antibiotic exposure by 6 months and asthma and allergy at 6 years: Findings in a cohort of 1,401 US children. Am. J. Epidemiol. 2011, 173, 310-318.
110. Jedrychowski, W.; Galas, A.; Whyatt, R.; Perera, F. The prenatal use of antibiotics and the development of allergic disease in one year old infants. A preliminary study. Int. J. Occup. Med. Environ. Health 2006, 19, 70-76.
111. Cho, I.; Yamanishi, S.; Cox, L.; Methe, B.A.; Zavadil, J.; Li, K.; Gao, Z.; Mahana, D.; Raju, K.; Teitler, I. et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 2012, 488, 621-626.
112. Sudo, N.; Yu, X.N.; Aiba, Y.; Oyama, N.; Sonoda, J.; Koga, Y.; Kubo, C. An oral introduction of intestinal bacteria prevents the development of a long-term Th2-skewed immunological memory induced by neonatal antibiotic treatment in mice. Clin. Exp. Allergy 2002, 32, 1112-1116.
113. Dimmitt, R.A.; Staley, E.M.; Chuang, G.; Tanner, S.M.; Soltau, T.D.; Lorenz, R.G. Role of postnatal acquisition of the intestinal microbiome in the early development of immune function. J. Pediatr. Gastroenterol. Nutr. 2010, 51, 262-273.
114. Wlodarska, M.; Willing, B.; Keeney, K.M.; Menendez, A.; Bergstrom, K.S.; Gill, N.; Russell, S.L.; Vallance, B.A.; Finlay, B.B. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect. Immun. 2011, 79, 1536-1545.
115. Fanaro, S.; Chierici, R.; Guerrini, P.; Vigi, V. Intestinal microflora in early infancy: Composition and development. Acta Paediatr. Suppl. 2003, 91, 48-55.
116. Adlerberth, I.; Lindberg, E.; Aberg, N.; Hesselmar, B.; Saalman, R.; Strannegard, I.L.; Wold, A.E. Reduced enterobacterial and increased staphylococcal colonization of the infantile bowel: An effect of hygienic lifestyle? Pediatr. Res. 2006, 59, 96-101.
117. Penders, J.; Thijs, C.; Vink, C.; Stelma, F.F.; Snijders, B.; Kummeling, I.; van den Brandt, P.A.; Stobberingh, E.E. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 2006, 118, 511-521.
118. Magne, F.; Abely, M.; Boyer, F.; Morville, P.; Pochart, P.; Suau, A. Low species diversity and high interindividual variability in faeces of preterm infants as revealed by sequences of 16S rRNA genes and PCR-temporal temperature gradient gel electrophoresis profiles. FEMS Microbiol. Ecol. 2006, 57, 128-138.
119. Jacquot, A.; Neveu, D.; Aujoulat, F.; Mercier, G.; Marchandin, H.; Jumas-Bilak, E.; Picaud, J.C. Dynamics and clinical evolution of bacterial gut microflora in extremely premature patients. J. Pediatr. 2011, 158, 390-396.
120. Arboleya, S.; Solis, G.; Fernandez, N.; de los Reyes-Gavilan, C.G.; Gueimonde, M. Facultative to strict anaerobes ratio in the preterm infant microbiota: A target for intervention? Gut Microbes 2012, 3, 583-588.
121. Sharma, R.; Young, C.; Neu, J. Molecular modulation of intestinal epithelial barrier: Contribution of microbiota. J. Biomed. Biotechnol. 2010, 2010, 305879.
122. Sherman, M.P. New concepts of microbial translocation in the neonatal intestine: Mechanisms and prevention. Clin. Perinatol. 2010, 37, 565-579.
123. Biasucci, G.; Benenati, B.; Morelli, L.; Bessi, E.; Boehm, G. Cesarean delivery may affect the early biodiversity of intestinal bacteria. J. Nutr. 2008, 138, 1796S-1800S.
124. Azad, M.B.; Konya, T.; Maughan, H.; Guttman, D.S.; Field, C.J.; Chari, R.S.; Sears, M.R.; Becker, A.B.; Scott, J.A.; Kozyrskyj, A.L. Gut microbiota of healthy Canadian infants: Profiles by mode of delivery and infant diet at 4 months. CMAJ 2013, 185, 385-394.
125. Salminen, S.; Gibson, G.R.; McCartney, A.L.; Isolauri, E. Influence of mode of delivery on gut microbiota composition in seven year old children. Gut 2004, 53, 1388-1389.
126. Malamitsi-Puchner, A.; Protonotariou, E.; Boutsikou, T.; Makrakis, E.; Sarandakou, A.; Creatsas, G. The influence of the mode of delivery on circulating cytokine concentrations in the perinatal period. Early Hum. Dev. 2005, 81, 387-392.
127. Decker, E.; Engelmann, G.; Findeisen, A.; Gerner, P.; Laass, M.; Ney, D.; Posovszky, C.; Hoy, L.; Hornef, M.W. Cesarean delivery is associated with celiac disease but not inflammatory bowel disease in children. Pediatrics 2010, 125, e1433-e1440.
128. Neu, J.; Rushing, J. Cesarean versus vaginal delivery: Long-term infant outcomes and the hygiene hypothesis. Clin. Perinatol. 2011, 38, 321-331.
129. Renz-Polster, H.; David, M.R.; Buist, A.S.; Vollmer, W.M.; O’Connor, E.A.; Frazier, E.A.; Wall, M.A. Caesarean section delivery and the risk of allergic disorders in childhood. Clin. Exp. Allergy 2005, 35, 1466-1472.
130. Eggesbo, M.; Botten, G.; Stigum, H.; Nafstad, P.; Magnus, P. Is delivery by cesarean section a risk factor for food allergy? J. Allergy Clin. Immunol. 2003, 112, 420-426.
131. 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, 317-321.
132. Coppa, G.V.; Bruni, S.; Morelli, L.; Soldi, S.; Gabrielli, O. The first prebiotics in humans: Human milk oligosaccharides. J. Clin. Gastroenterol. 2004, 38 (6 Suppl), S80-S83.
133. Field, C.J. The immunological components of human milk and their effect on immune development in infants. J. Nutr. 2005, 135, 1-4.
134. Iyengar, S.R.; Walker, W.A. Immune factors in breast milk and the development of atopic disease. J. Pediatr. Gastroenterol. Nutr. 2012, 55, 641-647.
135. Heikkila, M.P.; Saris, P.E. Inhibition of Staphylococcus aureus by the commensal bacteria of human milk. J. Appl. Microbiol. 2003, 95, 471-478.
136. Martin, R.; Langa, S.; Reviriego, C.; Jiminez, E.; Marin, M.L.; Xaus, J.; Fernandez, L.; Rodriguez, J.M. Human milk is a source of lactic acid bacteria for the infant gut. J. Pediatr. 2003, 143, 754-758.
137. Martin, R.; Jimenez, E.; Heilig, H.; Fernandez, L.; Marin, M.L.; Zoetendal, E.G.; Rodriguez, J.M. Isolation of bifidobacteria from breast milk and assessment of the bifidobacterial population by PCR-denaturing gradient gel electrophoresis and quantitative real-time PCR. Appl. Environ. Microbiol. 2009, 75, 965-969.
138. Gueimonde, M.; Laitinen, K.; Salminen, S.; Isolauri, E. Breast milk: A source of bifidobacteria for infant gut development and maturation? Neonatology 2007, 92, 64-66.
139. Jost, T.; Lacroix, C.; Braegger, C.; Chassard, C. Assessment of bacterial diversity in breast milk using culture-dependent and culture-independent approaches. Br. J. Nutr. 2013, 110, 1253-1262.
140. Collado, M.C.; Delgado, S.; Maldonado, A.; Rodriguez, J.M. Assessment of the bacterial diversity of breast milk of healthy women by quantitative real-time PCR. Lett. Appl. Microbiol. 2009, 48, 523-528.
141. Cabrera-Rubio, R.; Collado, M.C.; Laitinen, K.; Salminen, S.; Isolauri, E.; Mira, A. The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am. J. Clin. Nutr. 2012, 96, 544-551.
142. Ward, T.L.; Hosid, S.; Ioshikhes, I.; Altosaar, I. Human milk metagenome: A functional capacity analysis. BMC Microbiol. 2013, 13, 116.
143. Jeurink, P.V.; van Bergenhenegouwen, J.; Jimenez, E.; Knippels, L.M.; Fernandez, L.; Garssen, J.; Knol, J.; Rodriguez, J.M.; Martin, R. Human milk: A source of more life than we imagine. Benef. Microbes 2013, 4, 17-30.
144. Vidal, K.; Donnet-Hughes, A. CD14: A soluble pattern recognition receptor in milk. Adv. Exp. Med. Biol. 2008, 606, 195-216.
145. Brandtzaeg, P. Mucosal immunity: Integration between mother and the breast-fed infant. Vaccine 2003, 21, 3382-3388.
146. Dvorak, B.; Fituch, C.C.; Williams, C.S.; Hurst, N.M.; Schanler, R.J. Concentrations of epidermal growth factor and transforming growth factor-alpha in preterm milk. Adv. Exp. Med. Biol. 2004, 554, 407-409.
147. Sjogren, Y.M.; Tomicic, S.; Lundberg, A.; Bottcher, M.F.; Bjorksten, B.; Sverremark-Ekstrom, E.; Jenmalm, M.C. Influence of early gut microbiota on the maturation of childhood mucosal and systemic immune responses. Clin. Exp. Allergy 2009, 39, 1842-1851.
148. Chichlowski, M.; de Lartigue, G.; German, J.B.; Raybould, H.E.; Mills, D.A. Bifidobacteria isolated from infants and cultured on human milk oligosaccharides affect intestinal epithelial function. J. Pediatr. Gastroenterol. Nutr. 2012, 55, 321-327.
149. Hosea Blewett, H.J.; Cicalo, M.C.; Holland, C.D.; Field, C.J. The immunological components of human milk. Adv. Food Nutr. Res. 2008, 54, 45-80.
150. Orivuori, L.; Loss, G.; Roduit, C.; Dalphin, J.C.; Depner, M.; Genuneit, J.; Lauener, R.; Pekkanen, J.; Pfefferle, P.; Riedler, J. et al. Soluble immunoglobulin A in breast milk is inversely associated with atopic dermatitis at early age: The PASTURE cohort study. Clin. Exp. Allergy 2013, doi:10.1111/cea.12199.
151. Laiho, K.; Lampi, A.M.; Hamalainen, M.; Moilanen, E.; Piironen, V.; Arvola, T.; Syrjanen, S.; Isolauri, E. Breast milk fatty acids, eicosanoids, and cytokines in mothers with and without allergic disease. Pediatr. Res. 2003, 53, 642-647.
152. Van Odijk, J.; Kull, I.; Borres, M.P.; Brandtzaeg, P.; Edberg, U.; Hanson, L.A.; Host, A.; Kuitunen, M.; Olsen, S.F.; Skerfving, S. et al. Breastfeeding and allergic disease: A multidisciplinary review of the literature (1966-2001) on the mode of early feeding in infancy and its impact on later atopic manifestations. Allergy 2003, 58, 833-843.
153. Korotkova, M.; Telemo, E.; Hanson, L.A.; Strandvik, B. Modulation of neonatal immunological tolerance to ovalbumin by maternal essential fatty acid intake. Pediatr. Allergy Immunol. 2004, 15, 112-122.
154. Hanson, L.A.; Korotkova, M.; Telemo, E. Breast-feeding, infant formulas, and the immune system. Ann. Allergy Asthma Immunol. 2003, 90 (6 Suppl 3), 59-63.
155. Palmer, D.J.; Makrides, M. Diet of lactating women and allergic reactions in their infants. Curr. Opin. Clin. Nutr. Metab. Care 2006, 9, 284-288.
156. Kalliomaki, M.; Salminen, S.; Arvilommi, H.; Kero, P.; Koskinen, P.; Isolauri, E. Probiotics in primary prevention of atopic disease: A randomised placebo-controlled trial. Lancet 2001, 357, 1076-1079.
157. Kalliomaki, M.; Salminen, S.; Poussa, T.; Arvilommi, H.; Isolauri, E. Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial. Lancet 2003, 361, 1869-1871.
158. Kuitunen, M.; Kukkonen, K.; Juntunen-Backman, K.; Korpela, R.; Poussa, T.; Tuure, T.; Haahtela, T.; Savilahti, E. Probiotics prevent IgE-associated allergy until age 5 years in cesareandelivered children but not in the total cohort. J. Allergy Clin. Immunol. 2009, 123, 335-341.
159. Chichlowski, M.; German, J.B.; Lebrilla, C.B.; Mills, D.A. The influence of milk oligosaccharides on microbiota of infants: Opportunities for formulas. Annu. Rev. Food Sci. Technol. 2011, 2, 331-351.
160. Veereman-Wauters, G. Application of prebiotics in infant foods. Br. J. Nutr. 2005, 93 (Suppl. 1), S57-S60.
161. Rao, S.; Srinivasjois, R.; Patole, S. Prebiotic supplementation in full-term neonates: A systematic review of randomized controlled trials. Arch. Pediatr. Adolesc. Med. 2009, 163, 755-764.
162. Arslanoglu, S.; Moro, G.E.; Boehm, G. Early supplementation of prebiotic oligosaccharides protects formula-fed infants against infections during the first 6 months of life. J. Nutr. 2007, 137, 2420-2424.
163. Arslanoglu, S.; Moro, G.E.; Schmitt, J.; Tandoi, L.; Rizzardi, S.; Boehm, G. Early dietary intervention with a mixture of prebiotic oligosaccharides reduces the incidence of allergic manifestations and infections during the first two years of life. J. Nutr. 2008, 138, 1091-1095.
164. Mugambi, M.N.; Musekiwa, A.; Lombard, M.; Young, T.; Blaauw, R. Synbiotics, probiotics or prebiotics in infant formula for full term infants: A systematic review. Nutr J. 2012, 11, 81.
165. Fanaro, S.; Boehm, G.; Garssen, J.; Knol, J.; Mosca, F.; Stahl, B.; Vigi, V. Galacto-oligosaccharides and long-chain fructo-oligosaccharides as prebiotics in infant formulas: A review. Acta Paediatr. Suppl. 2005, 94, 22-26.
166. Garrido, D.; Kim, J.H.; German, J.B.; Raybould, H.E.; Mills, D.A. Oligosaccharide binding proteins from Bifidobacterium longum subsp. infantis reveal a preference for host glycans. PLoS One 2011, 6, e17315.
167. Crittenden, R.; Playne, M.J. Prebiotics. In Handbook of Probiotics and Prebiotics; Lee, Y., Salminen, S., Eds.; John Wiley Sons: Hoboken, NJ, USA, 2009; pp. 535-581.
168. Nakamura, T.; Urashima, T. The milk oligosaccharides of domestic farm animals. Trends Glycosci. Glycotechnol. 2004, 16, 135-142.
169. Ninonuevo, M.R.; Park, Y.; Yin, H.; Zhang, J.; Ward, R.E.; Clowers, B.H.; German, J.B.; Freeman, S.L.; Killeen, K.; Grimm, R. et al. A strategy for annotating the human milk glycome. J. Agric. Food Chem. 2006, 54, 7471-7480.
170. Tao, N.; DePeters, E.J.; German, J.B.; Grimm, R.; Lebrilla, C.B. Variations in bovine milk oligosaccharides during early and middle lactation stages analyzed by high-performance liquid chromatography-chip/mass spectrometry. J. Dairy Sci. 2009, 92, 2991-3001.
171. Lara-Villoslada, F.; Debras, E.; Nieto, A.; Concha, A.; Galvez, J.; Lopez-Huertas, E.; Boza, J.; Obled, C.; Xaus, J. Oligosaccharides isolated from goat milk reduce intestinal inflammation in a rat model of dextran sodium sulfate-induced colitis. Clin. Nutr. 2006, 25, 477-488.