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The developing gut microbiota and its consequences for health

Published online by Cambridge University Press:  22 March 2018

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

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.

Type
Review
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

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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.CrossRefGoogle ScholarPubMed
2. Qin, J, Li, R, Raes, J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010; 464, 5965.CrossRefGoogle ScholarPubMed
3. Dietert, RR, Dietert, JM. The microbiome and sustainable healthcare. Healthcare (Basel). 2015; 3, 100129.Google Scholar
4. Jones, ML, Ganopolsky, JG, Martoni, CJ, Labbe, A, Prakash, S. Emerging science of the human microbiome. Gut Microbes. 2014; 5, 446457.CrossRefGoogle ScholarPubMed
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, 435454.CrossRefGoogle ScholarPubMed
6. Neish, AS. Microbes in gastrointestinal health and disease. Gastroenterology. 2009; 136, 6580.CrossRefGoogle ScholarPubMed
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, 1520.CrossRefGoogle ScholarPubMed
8. Gritz, EC, Bhandari, V. The human neonatal gut microbiome: a brief review. Front Pediatr. 2015; 3, 17.Google ScholarPubMed
9. Palmer, C, Bik, EM, Digiulio, DB, Relman, DA, Brown, PO. Development of the human infant intestinal microbiota. PLoS Biol. 2007; 5, e177.CrossRefGoogle ScholarPubMed
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, 28912904.CrossRefGoogle ScholarPubMed
11. Fitzstevens, JL, Smith, KC, Hagadorn, JI, et al. Systematic review of the human milk microbiota. Nutr Clin Pract. 2017; 32, 354364.CrossRefGoogle ScholarPubMed
12. Yatsunenko, T, Rey, FE, Manary, MJ, et al. Human gut microbiome viewed across age and geography. Nature. 2012; 486, 222227.CrossRefGoogle ScholarPubMed
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), 1315.CrossRefGoogle ScholarPubMed
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, 1197111975.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 385394.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 167172.CrossRefGoogle ScholarPubMed
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, 314326.CrossRefGoogle ScholarPubMed
21. Guaraldi, F, Salvatori, G. Effect of breast and formula feeding on gut microbiota shaping in newborns. Front Cell Infect Microbiol. 2012; 2, 94.CrossRefGoogle ScholarPubMed
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, 426437.CrossRefGoogle ScholarPubMed
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, 561S571S.CrossRefGoogle ScholarPubMed
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, 8087.CrossRefGoogle ScholarPubMed
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, 58115820.CrossRefGoogle ScholarPubMed
26. Gibson, MK, Crofts, TS, Dantas, G. Antibiotics and the developing infant gut microbiota and resistome. Curr Opin Microbiol. 2015; 27, 5156.CrossRefGoogle ScholarPubMed
27. Arboleya, S, Sanchez, B, Milani, C, et al. Intestinal microbiota development in preterm neonates and effect of perinatal antibiotics. J Pediatr. 2015; 166, 538544.CrossRefGoogle ScholarPubMed
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, 51845188.CrossRefGoogle ScholarPubMed
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, 1252212527.CrossRefGoogle ScholarPubMed
30. Aujoulat, F, Roudiere, L, Picaud, JC, et al. Temporal dynamics of the very premature infant gut dominant microbiota. BMC Microbiol. 2014; 14, 325.CrossRefGoogle ScholarPubMed
31. Groer, MW, Luciano, AA, Dishaw, LJ, et al. Development of the preterm infant gut microbiome: a research priority. Microbiome. 2014; 2, 38.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 821830.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, 11071115.CrossRefGoogle ScholarPubMed
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, 7784.CrossRefGoogle ScholarPubMed
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, 414.CrossRefGoogle 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, 329332.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 2025.CrossRefGoogle ScholarPubMed
40. Adkins, B, Leclerc, C, Marshall-Clarke, S. Neonatal adaptive immunity comes of age. Nat Rev Immunol. 2004; 4, 553564.CrossRefGoogle ScholarPubMed
41. Quigley, EM. Leaky gut – concept or clinical entity? Curr Opin Gastroenterol. 2016; 32, 7479.CrossRefGoogle ScholarPubMed
42. Ohnmacht, C. Microbiota, regulatory T cell subsets, and allergic disorders. Allergo J Int. 2016; 25, 114123.CrossRefGoogle ScholarPubMed
43. Okada, H, Kuhn, C, Feillet, H, Bach, JF. The ‘hygiene hypothesis’ for autoimmune and allergic diseases: an update. Clin. Exp. Immunol. 2010; 160, 19.CrossRefGoogle ScholarPubMed
44. Gensollen, T, Iyer, SS, Kasper, DL, Blumberg, RS. How colonization by microbiota in early life shapes the immune system. Science. 2016; 352, 539544.CrossRefGoogle ScholarPubMed
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, 982989.CrossRefGoogle ScholarPubMed
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, 8594.CrossRefGoogle ScholarPubMed
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, 983991.CrossRefGoogle ScholarPubMed
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, 468472.CrossRefGoogle ScholarPubMed
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, 1625.CrossRefGoogle ScholarPubMed
50. Bager, P, Wohlfahrt, J, Westergaard, T. Caesarean delivery and risk of atopy and allergic disease: meta-analyses. Clin Exp Allergy. 2008; 38, 634642.CrossRefGoogle ScholarPubMed
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, 792800.CrossRefGoogle ScholarPubMed
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, 636638.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
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, 465473.CrossRefGoogle ScholarPubMed
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, 201212.CrossRefGoogle ScholarPubMed
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, e394e400.CrossRefGoogle ScholarPubMed
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, 177188.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
59. Blazquez, AB, Berin, MC. Microbiome and food allergy. Transl Res. 2017; 179, 199203.CrossRefGoogle ScholarPubMed
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, 842850.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 21992207.CrossRefGoogle ScholarPubMed
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, 610616.CrossRefGoogle ScholarPubMed
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, 522529.CrossRefGoogle 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, 7785.CrossRefGoogle ScholarPubMed
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, 12901298.CrossRefGoogle ScholarPubMed
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, 705721.CrossRefGoogle ScholarPubMed
68. Wen, L, Duffy, A. Factors influencing the gut microbiota, inflammation, and type 2 diabetes. J Nutr. 2017; 147, 1468S1475S.CrossRefGoogle ScholarPubMed
69. Foster, JA, Rinaman, L, Cryan, JF. Stress & the gut-brain axis: regulation by the microbiome. Neurobiol Stress. 2017; 7, 124136.CrossRefGoogle ScholarPubMed
70. Rieder, R, Wisniewski, PJ, Alderman, BL, Campbell, SC. Microbes and mental health: a review. Brain Behav Immun. 2017; 66, 917.CrossRefGoogle ScholarPubMed
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, 984995.CrossRefGoogle ScholarPubMed
72. Vuong, HE, Hsiao, EY. Emerging roles for the gut microbiome in autism spectrum disorder. Biol Psychiatry. 2017; 81, 411423.CrossRefGoogle ScholarPubMed
73. Yang, Y, Tian, J, Yang, B. Targeting gut microbiome: a novel and potential therapy for autism. Life Sci. 2017; 194, 111119.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, 410417.CrossRefGoogle ScholarPubMed
75. Jimenez, E, Marin, ML, Martin, R, et al. Is meconium from healthy newborns actually sterile? Res Microbiol. 2008; 159, 187193.CrossRefGoogle ScholarPubMed
76. Aagaard, K, Ma, J, Antony, KM, et al. The placenta harbors a unique microbiome. Sci Transl Med. 2014; 6, 237ra65.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 226227.CrossRefGoogle ScholarPubMed
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, 3847.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
81. Pettker, CM, Buhimschi, IA, Magloire, LK, et al. Value of placental microbial evaluation in diagnosing intra-amniotic infection. Obstet Gynecol. 2007; 109, 739749.CrossRefGoogle ScholarPubMed
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 e651616.CrossRefGoogle ScholarPubMed
83. Cao, B, Stout, MJ, Lee, I, Mysorekar, IU. Placental microbiome and its role in preterm birth. Neoreviews. 2014; 15, e537e545.CrossRefGoogle ScholarPubMed
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 e1627 e16.CrossRefGoogle ScholarPubMed
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, 69246937.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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, 1106011065.CrossRefGoogle ScholarPubMed
89. Nuriel-Ohayon, M, Neuman, H, Koren, O. Microbial changes during pregnancy, birth, and infancy. Front Microbiol. 2016; 7, 1031.CrossRefGoogle ScholarPubMed
90. Koren, O, Goodrich, JK, Cullender, TC, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012; 150, 470480.CrossRefGoogle ScholarPubMed
91. Gomez de Aguero, M, Ganal-Vonarburg, SC, Fuhrer, T, et al. The maternal microbiota drives early postnatal innate immune development. Science. 2016; 351, 12961302.CrossRefGoogle ScholarPubMed
92. Abrahamsson, TR, Wu, RY, Jenmalm, MC. Gut microbiota and allergy: the importance of the pregnancy period. Pediatr Res. 2015; 77, 214219.CrossRefGoogle ScholarPubMed
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, 894899.CrossRefGoogle ScholarPubMed
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, 491502.Google ScholarPubMed
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, 506514.CrossRefGoogle ScholarPubMed
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, 353362.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 14681477.CrossRefGoogle ScholarPubMed
100. Sohn, K, Underwood, MA. Prenatal and postnatal administration of prebiotics and probiotics. Semin Fetal Neonatal Med. 2017; 22, 284289.CrossRefGoogle ScholarPubMed
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