Hostname: page-component-6bf8c574d5-k2jvg Total loading time: 0 Render date: 2025-03-07T03:19:25.674Z Has data issue: false hasContentIssue false
  • English
  • Français

The developing gut microbiota and its consequences for health

Part of: French DOHaD J DOHaD 10th Anniversary Collection DOHaD on International Women's Day 2020

Published online by Cambridge University Press:  22 March 2018

M.-J. Butel ,
A.-J. Waligora-Dupriet  and
S. Wydau-Dematteis
M.-J. Butel*
Affiliation:
Paris Descartes University, Sorbonne Paris Cité, Faculty of pharmacy, Hospital-University Department «Risk in pregnancy», Team “Intestinal ecosystem, Probiotics, Antibiotics”, Paris, France
A.-J. Waligora-Dupriet
Affiliation:
Paris Descartes University, Sorbonne Paris Cité, Faculty of pharmacy, Hospital-University Department «Risk in pregnancy», Team “Intestinal ecosystem, Probiotics, Antibiotics”, Paris, France
S. Wydau-Dematteis
Affiliation:
Paris Descartes University, Sorbonne Paris Cité, Faculty of pharmacy, Hospital-University Department «Risk in pregnancy», Team “Intestinal ecosystem, Probiotics, Antibiotics”, Paris, France
*
Address for correspondence: M.-J. Butel, Faculté de Pharmacie, EA 4065, 4 avenue de l’Observatoire, Paris 75006, France. E-mail: marie-jose.butel@parisdescartes.fr
Get access Rights & Permissions [Opens in a new window]

Abstract

The developmental origin of health and disease highlights the importance of the period of the first 1000 days (from the conception to the 2 years of life). The process of the gut microbiota establishment is included in this time window. Various perinatal determinants, such as cesarean section delivery, type of feeding, antibiotics treatment, gestational age or environment, can affect the pattern of bacterial colonization and result in dysbiosis. The alteration of the early bacterial gut pattern can persist over several months and may have long-lasting functional effects with an impact on disease risk later in life. As for example, early gut dysbiosis has been involved in allergic diseases and obesity occurrence. Besides, while it was thought that the fetus developed under sterile conditions, recent data suggested the presence of a microbiota in utero, particularly in the placenta. Even if the origin of this microbiota and its eventual transfer to the infant are nowadays unknown, this placental microbiota could trigger immune responses in the fetus and would program the infant’s immune development during fetal life, earlier than previously considered. Moreover, several studies demonstrated a link between the composition of placental microbiota and some pathological conditions of the pregnancy. All these data show the evidence of relationships between the neonatal gut establishment and future health outcomes. Hence, the use of pre- and/or probiotics to prevent or repair any early dysbiosis is increasingly attractive to avoid long-term health consequences.

Keywords

gut microbiotaneonatesestablishmenthealthdiseases
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 9 , Issue 6 , December 2018 , pp. 590 - 597
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Sender, R, Fuchs, S, Milo, R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016; 14, e1002533.Google Scholar
2. Qin, J, Li, R, Raes, J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010; 464, 59–65.Google Scholar
3. Dietert, RR, Dietert, JM. The microbiome and sustainable healthcare. Healthcare (Basel). 2015; 3, 100–129.Google Scholar
4. Jones, ML, Ganopolsky, JG, Martoni, CJ, Labbe, A, Prakash, S. Emerging science of the human microbiome. Gut Microbes. 2014; 5, 446–457.Google Scholar
5. Fujimura, KE, Slusher, NA, Cabana, MD, Lynch, SV. Role of the gut microbiota in defining human health. Expert Rev Anti Infect Ther. 2010; 8, 435–454.Google Scholar
6. Neish, AS. Microbes in gastrointestinal health and disease. Gastroenterology. 2009; 136, 65–80.Google Scholar
7. Charles, MA, Delpierre, C, Breant, B. Developmental origin of health and adult diseases (dohad): evolution of a concept over three decades. Med Sci (Paris). 2016; 32, 15–20.Google Scholar
8. Gritz, EC, Bhandari, V. The human neonatal gut microbiome: a brief review. Front Pediatr. 2015; 3, 17.Google Scholar
9. Palmer, C, Bik, EM, Digiulio, DB, Relman, DA, Brown, PO. Development of the human infant intestinal microbiota. PLoS Biol. 2007; 5, e177.Google Scholar
10. Jost, T, Lacroix, C, Braegger, CP, Rochat, F, Chassard, C. Vertical mother-neonate transfer of maternal gut bacteria via breastfeeding. Environ Microbiol. 2014; 16, 2891–2904.Google Scholar
11. Fitzstevens, JL, Smith, KC, Hagadorn, JI, et al. Systematic review of the human milk microbiota. Nutr Clin Pract. 2017; 32, 354–364.Google Scholar
12. Yatsunenko, T, Rey, FE, Manary, MJ, et al. Human gut microbiome viewed across age and geography. Nature. 2012; 486, 222–227.Google Scholar
13. Biasucci, G, Rubini, M, Riboni, S, et al. Mode of delivery affects the bacterial community in the newborn gut. Early Hum Dev. 2010; 86(Suppl. 1), 13–15.Google Scholar
14. Dominguez-Bello, MG, Costello, EK, Contreras, M, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010; 107, 11971–11975.Google Scholar
15. Rutayisire, E, Huang, K, Liu, Y, Tao, F. The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants’ life: a systematic review. BMC Gastroenterol. 2016; 16, 86.Google Scholar
16. Martin, R, Makino, H, Cetinyurek Yavuz, A, et al. Early-life events, including mode of delivery and type of feeding, siblings and gender, shape the developing gut microbiota. PLoS One. 2016; 11, e0158498.Google Scholar
17. Azad, MB, Konya, T, Maughan, H, et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ. 2013; 185, 385–394.Google Scholar
18. Backhed, F, Roswall, J, Peng, Y, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015; 17, 852.Google Scholar
19. Goedert, JJ, Hua, X, Yu, G, Shi, J. Diversity and composition of the adult fecal microbiome associated with history of cesarean birth or appendectomy: analysis of the American gut project. EBioMedicine. 2014; 1, 167–172.Google Scholar
20. Chu, DM, Ma, J, Prince, AL, et al. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nature Med. 2017; 23, 314–326.Google Scholar
21. Guaraldi, F, Salvatori, G. Effect of breast and formula feeding on gut microbiota shaping in newborns. Front Cell Infect Microbiol. 2012; 2, 94.Google Scholar
22. Jost, T, Lacroix, C, Braegger, C, Chassard, C. Impact of human milk bacteria and oligosaccharides on neonatal gut microbiota establishment and gut health. Nutr Rev. 2015; 73, 426–437.Google Scholar
23. Oozeer, R, van, LK, Ludwig, T, et al. Intestinal microbiology in early life: specific prebiotics can have similar functionalities as human-milk oligosaccharides. Am J Clin Nutr. 2013; 98, 561S–571S.Google Scholar
24. Tanaka, S, Kobayashi, T, Songjinda, P, et al. Influence of antibiotic exposure in the early postnatal period on the development of intestinal microbiota. FEMS Immunol Med Microbiol. 2009; 56, 80–87.Google Scholar
25. Fouhy, F, Guinane, CM, Hussey, S, et al. 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.Google Scholar
26. Gibson, MK, Crofts, TS, Dantas, G. Antibiotics and the developing infant gut microbiota and resistome. Curr Opin Microbiol. 2015; 27, 51–56.Google Scholar
27. Arboleya, S, Sanchez, B, Milani, C, et al. Intestinal microbiota development in preterm neonates and effect of perinatal antibiotics. J Pediatr. 2015; 166, 538–544.Google Scholar
28. Jaureguy, F, Carton, M, Panel, P, et al. Effects of intrapartum prophylaxis on the intestinal bacterial colonization in infants. J Clin Microbiol. 2004; 42, 5184–5188.Google Scholar
29. La Rosa, PS, Warner, BB, Zhou, Y, et al. Patterned progression of bacterial populations in the premature infant gut. Proc Natl Acad Sci U S A. 2014; 111, 12522–12527.Google Scholar
30. Aujoulat, F, Roudiere, L, Picaud, JC, et al. Temporal dynamics of the very premature infant gut dominant microbiota. BMC Microbiol. 2014; 14, 325.Google Scholar
31. Groer, MW, Luciano, AA, Dishaw, LJ, et al. Development of the preterm infant gut microbiome: a research priority. Microbiome. 2014; 2, 38.Google Scholar
32. Ferraris, L, Butel, MJ, Campeotto, F, et al. Clostridia in premature neonates’ gut: incidence, antibiotic susceptibility, and perinatal determinants influencing colonization. PLoS One. 2012; 7, e30594.Google Scholar
33. Roze, JC, Ancel, PY, Lepage, P, et al. Nutritional strategies and gut microbiota composition as risk factors for necrotizing enterocolitis in very-preterm infants. Am J Clin Nutr. 2017; 106, 821–830.Google Scholar
34. Cassir, N, Benamar, S, Khalil, JB, et al. Clostridium butyricum strains and dysbiosis linked to necrotizing enterocolitis in preterm neonates. Clin Infect Dis. 2015; 61, 1107–1115.Google Scholar
35. Fallani, M, Young, D, Scott, J, et al. Intestinal microbiota of 6-week-old infants across Europe: geographic influence beyond delivery mode, breast-feeding, and antibiotics. J Pediatr Gastroenterol Nutr. 2010; 51, 77–84.Google Scholar
36. Itani, T, Ayoub Moubareck, C, Melki, I, et al. Establishment and development of the intestinal microbiota of preterm infants in a Lebanese tertiary hospital. Anaerobe. 2017; 43, 4–14.Google Scholar
37. Kemppainen, KM, Ardissone, AN, Davis-Richardson, AG, et al. Early childhood gut microbiomes show strong geographic differences among subjects at high risk for type 1 diabetes. Diabetes Care. 2015; 38, 329–332.Google Scholar
38. Neu, J. Developmental aspects of maternal-fetal, and infant gut microbiota and implications for long-term health. Matern Health Neonatol Perinatol. 2015; 1, 6.Google Scholar
39. Kuzniewicz, MW, Wi, S, Qian, Y, et al. Prevalence and neonatal factors associated with autism spectrum disorders in preterm infants. J Pediatr. 2014; 164, 20–25.Google Scholar
40. Adkins, B, Leclerc, C, Marshall-Clarke, S. Neonatal adaptive immunity comes of age. Nat Rev Immunol. 2004; 4, 553–564.Google Scholar
41. Quigley, EM. Leaky gut – concept or clinical entity? Curr Opin Gastroenterol. 2016; 32, 74–79.Google Scholar
42. Ohnmacht, C. Microbiota, regulatory T cell subsets, and allergic disorders. Allergo J Int. 2016; 25, 114–123.Google Scholar
43. Okada, H, Kuhn, C, Feillet, H, Bach, JF. The ‘hygiene hypothesis’ for autoimmune and allergic diseases: an update. Clin. Exp. Immunol. 2010; 160, 1–9.Google Scholar
44. Gensollen, T, Iyer, SS, Kasper, DL, Blumberg, RS. How colonization by microbiota in early life shapes the immune system. Science. 2016; 352, 539–544.Google Scholar
45. Foliaki, S, Pearce, N, Bjorksten, B, et al. 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.Google Scholar
46. Pitter, G, Ludvigsson, JF, Romor, P, et al. Antibiotic exposure in the first year of life and later treated asthma, a population based birth cohort study of 143,000 children. Eur J Epidemiol. 2016; 31, 85–94.Google Scholar
47. Tsakok, T, McKeever, TM, Yeo, L, Flohr, C. Does early life exposure to antibiotics increase the risk of eczema? A systematic review. Br J Dermatol. 2013; 169, 983–991.Google Scholar
48. Alm, B, Goksor, E, Pettersson, R, et al. Antibiotics in the first week of life is a risk factor for allergic rhinitis at school age. Pediatr Allergy Immunol. 2014; 25, 468–472.Google Scholar
49. Huang, L, Chen, Q, Zhao, Y, et al. Is elective cesarean section associated with a higher risk of asthma? A meta-analysis. J Asthma. 2015; 52, 16–25.Google Scholar
50. Bager, P, Wohlfahrt, J, Westergaard, T. Caesarean delivery and risk of atopy and allergic disease: meta-analyses. Clin Exp Allergy. 2008; 38, 634–642.Google Scholar
51. Gabet, S, Just, J, Couderc, R, Seta, N, Momas, I. Allergic sensitisation in early childhood: patterns and related factors in PARIS birth cohort. Int J Hyg Environ Health. 2016; 219, 792–800.Google Scholar
52. Loo, EXL, Sim, JZT, Loy, SL, et al. Associations between caesarean delivery and allergic outcomes: results from the gusto study. Ann Allergy Asthma Immunol. 2017; 118, 636–638.Google Scholar
53. Brix, N, Stokholm, L, Jonsdottir, F, Kristensen, K, Secher, NJ. Comparable risk of childhood asthma after vaginal delivery and emergency caesarean section. Dan Med J. 2017; 64, pii: A5313.Google Scholar
54. Rusconi, F, Zugna, D, Annesi-Maesano, I, et al. Mode of delivery and asthma at school age in 9 European birth cohorts. Am J Epidemiol. 2017; 185, 465–473.Google Scholar
55. Noval Rivas, M, Burton, OT, Wise, P, et al. A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis. J Allergy Clin Immunol. 2013; 131, 201–212.Google Scholar
56. Thompson-Chagoyan, OC, Vieites, JM, Maldonado, J, Edwards, C, Gil, A. Changes in faecal microbiota of infants with cow’s milk protein allergy – a Spanish prospective case-control 6-month follow-up study. Pediatr Allergy Immunol. 2010; 21, e394–e400.Google Scholar
57. Melli, LC, do Carmo-Rodrigues, MS, Araujo-Filho, HB, Sole, D, de Morais, MB. Intestinal microbiota and allergic diseases: a systematic review. Allergol Immunopathol (Madr). 2016; 44, 177–188.Google Scholar
58. Vael, C, Vanheirstraeten, L, Desager, KN, Goossens, H. Denaturing gradient gel electrophoresis of neonatal intestinal microbiota in relation to the development of asthma. BMC Microbiol. 2011; 11, 68.Google Scholar
59. Blazquez, AB, Berin, MC. Microbiome and food allergy. Transl Res. 2017; 179, 199–203.Google Scholar
60. Abrahamsson, TR, Jakobsson, HE, Andersson, AF, et al. Low gut microbiota diversity in early infancy precedes asthma at school age. Clin Exp Allergy. 2014; 44, 842–850.Google Scholar
61. Arrieta, MC, Stiemsma, LT, Dimitriu, PA, et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci Transl Med. 2015; 7, 307ra152.Google Scholar
62. Stiemsma, LT, Arrieta, MC, Dimitriu, PA, et al. Shifts in Lachnospira and Clostridium sp. in the 3-month stool microbiome are associated with preschool age asthma. Clin Sci (Lond). 2016; 130, 2199–2207.Google Scholar
63. Huh, SY, Rifas-Shiman, SL, Zera, CA, et al. Delivery by caesarean section and risk of obesity in preschool age children: a prospective cohort study. Arch Dis Child. 2012; 97, 610–616.Google Scholar
64. Ajslev, TA, Andersen, CS, Gamborg, M, Sorensen, TI, Jess, T. Childhood overweight after establishment of the gut microbiota: the role of delivery mode, pre-pregnancy weight and early administration of antibiotics. Int J Obes (Lond). 2011; 35, 522–529.Google Scholar
65. Collado, MC, Laitinen, K, Salminen, S, Isolauri, E. Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk. Pediatr Res. 2012; 72, 77–85.Google Scholar
66. Azad, MB, Bridgman, SL, Becker, AB, Kozyrskyj, AL. Infant antibiotic exposure and the development of childhood overweight and central adiposity. Int J Obes (Lond). 2014; 38, 1290–1298.Google Scholar
67. Cox, LM, Yamanishi, S, Sohn, J, et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell. 2014; 158, 705–721.Google Scholar
68. Wen, L, Duffy, A. Factors influencing the gut microbiota, inflammation, and type 2 diabetes. J Nutr. 2017; 147, 1468S–1475S.Google Scholar
69. Foster, JA, Rinaman, L, Cryan, JF. Stress & the gut-brain axis: regulation by the microbiome. Neurobiol Stress. 2017; 7, 124–136.Google Scholar
70. Rieder, R, Wisniewski, PJ, Alderman, BL, Campbell, SC. Microbes and mental health: a review. Brain Behav Immun. 2017; 66, 9–17.Google Scholar
71. Petra, AI, Panagiotidou, S, Hatziagelaki, E, et al. Gut-microbiota-brain axis and its effect on neuropsychiatric disorders with suspected immune dysregulation. Clin Ther. 2015; 37, 984–995.Google Scholar
72. Vuong, HE, Hsiao, EY. Emerging roles for the gut microbiome in autism spectrum disorder. Biol Psychiatry. 2017; 81, 411–423.Google Scholar
73. Yang, Y, Tian, J, Yang, B. Targeting gut microbiome: a novel and potential therapy for autism. Life Sci. 2017; 194, 111–119.Google Scholar
74. Diaz Heijtz, R. Fetal, neonatal, and infant microbiome: perturbations and subsequent effects on brain development and behavior. Semin Fetal Neonatal Med. 2016; 21, 410–417.Google Scholar
75. Jimenez, E, Marin, ML, Martin, R, et al. Is meconium from healthy newborns actually sterile? Res Microbiol. 2008; 159, 187–193.Google Scholar
76. Aagaard, K, Ma, J, Antony, KM, et al. The placenta harbors a unique microbiome. Sci Transl Med. 2014; 6, 237ra65.Google Scholar
77. Collado, MC, Rautava, S, Aakko, J, Isolauri, E, Salminen, S. Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Sci Rep. 2016; 6, 23129.Google Scholar
78. Stout, MJ, Conlon, B, Landeau, M, 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, 226–227.Google Scholar
79. Han, YW, Shen, T, Chung, P, Buhimschi, IA, Buhimschi, CS. Uncultivated bacteria as etiologic agents of intra-amniotic inflammation leading to preterm birth. J Clin Microbiol. 2009; 47, 38–47.Google Scholar
80. Doyle, RM, Harris, K, Kamiza, S, et al. Bacterial communities found in placental tissues are associated with severe chorioamnionitis and adverse birth outcomes. PLoS One. 2017; 12, e0180167.Google Scholar
81. Pettker, CM, Buhimschi, IA, Magloire, LK, et al. Value of placental microbial evaluation in diagnosing intra-amniotic infection. Obstet Gynecol. 2007; 109, 739–749.Google Scholar
82. Antony, KM, Ma, J, Mitchell, KB, et al. The preterm placental microbiome varies in association with excess maternal gestational weight gain. Am J Obstet Gynecol. 2015; 212, 653 e651–616.Google Scholar
83. Cao, B, Stout, MJ, Lee, I, Mysorekar, IU. Placental microbiome and its role in preterm birth. Neoreviews. 2014; 15, e537–e545.Google Scholar
84. Prince, AL, Ma, J, Kannan, PS, et al. The placental membrane microbiome is altered among subjects with spontaneous preterm birth with and without chorioamnionitis. Am J Obstet Gynecol. 2016; 214, 627 e1–627 e16.Google Scholar
85. Zheng, J, Xiao, X, Zhang, Q, et al. The placental microbiome varies in association with low birth weight in full-term neonates. Nutrients. 2015; 7, 6924–6937.Google Scholar
86. Zheng, J, Xiao, X, Zhang, Q, et al. The placental microbiota is altered among subjects with gestational diabetes mellitus: a pilot study. Front Physiol. 2017; 8, 675.Google Scholar
87. Perez-Munoz, ME, Arrieta, MC, Ramer-Tait, AE, Walter, J. A critical assessment of the ‘sterile womb’ and ‘in utero colonization’ hypotheses: implications for research on the pioneer infant microbiome. Microbiome. 2017; 5, 48.Google Scholar
88. Digiulio, DB, Callahan, BJ, McMurdie, PJ, et al. Temporal and spatial variation of the human microbiota during pregnancy. Proc Natl Acad Sci U S A. 2015; 112, 11060–11065.Google Scholar
89. Nuriel-Ohayon, M, Neuman, H, Koren, O. Microbial changes during pregnancy, birth, and infancy. Front Microbiol. 2016; 7, 1031.Google Scholar
90. Koren, O, Goodrich, JK, Cullender, TC, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012; 150, 470–480.Google Scholar
91. Gomez de Aguero, M, Ganal-Vonarburg, SC, Fuhrer, T, et al. The maternal microbiota drives early postnatal innate immune development. Science. 2016; 351, 1296–1302.Google Scholar
92. Abrahamsson, TR, Wu, RY, Jenmalm, MC. Gut microbiota and allergy: the importance of the pregnancy period. Pediatr Res. 2015; 77, 214–219.Google Scholar
93. Collado, MC, Isolauri, E, Laitinen, K, Salminen, S. Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am J Clin Nutr. 2008; 88, 894–899.Google Scholar
94. Gibson, GR, Hutkins, R, Sanders, ME, et al. Expert consensus document: the international scientific association for probiotics and prebiotics (isapp) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017; 14, 491–502.Google Scholar
95. Hill, C, Guarner, F, Reid, G, et al. 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 . 2014; 11, 506–514.Google Scholar
96. Reid, G, Kumar, H, Khan, AI, et al. The case in favour of probiotics before, during and after pregnancy: insights from the first 1,500 days. Benef Microbes. 2016; 7, 353–362.Google Scholar
97. Alfaleh, K, Anabrees, J. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst Rev. 2014; 4, CD005496.Google Scholar
98. Fiocchi, A, Pawankar, R, Cuello-Garcia, C, et al. World Allergy Organization-Mcmaster university guidelines for allergic disease prevention (GLAD-P): probiotics. World Allergy Organ J. 2015; 8, 4.Google Scholar
99. Cuello-Garcia, C, Fiocchi, A, Pawankar, R, et al. Prebiotics for the prevention of allergies: a systematic review and meta-analysis of randomized controlled trials. Clin Exp Allergy. 2017; 47, 1468–1477.Google Scholar
100. Sohn, K, Underwood, MA. Prenatal and postnatal administration of prebiotics and probiotics. Semin Fetal Neonatal Med. 2017; 22, 284–289.Google Scholar