Intervention strategies for cesarean section- induced alterations in the microbiota-gut-brain axis

Nutrition Reviews

Volumn 75, Issue 4, 2017, Pages 225-240

  Moya Pérez, Angela ^a   Luczynski, Pauline ^a   Renes, Ingrid B ^c   Wang, Shugui ^d   Borre, Yuliya ^a   Ryan, C Anthony ^a,b   Knol, Jan ^c,e   Stanton, Catherine ^a,f   Dinan, Timothy G ^a,b   Cryan, John F ^b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c DANONE NUTRICIA RESEARCH   (Netherlands)

^d Danone Research Centre for Specialised Nutrition   (Singapore)

^e WAGENINGEN UNIVERSITY   (Netherlands)

^f TEAGASC FOOD RESEARCH CENTRE   (Ireland)

Author keywords

Cesarean section; Immunity; Metabolism; Microbiota; Prebiotics; Probiotics

Indexed keywords

FATTY ACID; PREBIOTIC AGENT; PROBIOTIC AGENT; SYNBIOTIC AGENT;

ARTICLE; ARTIFICIAL MILK; BACTERIAL MICROBIOME; BACTERIUM; BLOOD BRAIN BARRIER; BREAST FEEDING; BREAST MILK; CENTRAL NERVOUS SYSTEM FUNCTION; CESAREAN SECTION; EXPECTANT MOTHER; GASTROINTESTINAL TRACT; GESTATIONAL AGE; HEALTH STATUS; HUMAN; INFANT FEEDING; INTESTINE FLORA; MICROBIAL COLONIZATION; NERVE CELL DIFFERENTIATION; PERINATAL PERIOD; PHYSIOLOGICAL PROCESS; VERTICAL TRANSMISSION; BRAIN; FEMALE; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; PREGNANCY;

BRAIN; CESAREAN SECTION; FEMALE; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; PREGNANCY;

EID: 85020195314     PISSN: 00296643     EISSN: 17534887     Source Type: Journal    
DOI: 10.1093/nutrit/nuw069     Document Type: Article

References (180)

1. Hooper L V, Gordon JI. Commensal host-bacterial relationships in the gut. Science. 2001;292:1115-1118.
2. Nicholson J, Holmes E, Kinross J, et al. Host-gut microbiota metabolic interactions. Science. 2012;336:1262-1267.
3. Backhed F, Ley RE, Sonnenburg JL, et al. Host-bacterial mutualism in the human intestine. Science. 2005;307:1915-1920.
4. Hooper L V, Macpherson AJ. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol. 2010;10:159-169.
5. Rhee SH, Pothoulakis C, Mayer EA. Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat Rev Gastroenterol Hepatol. 2009;6:306-314.
6. Collins SM, Surette M, Bercik P. The interplay between the intestinal microbiota and the brain. Nat Rev Micro. 2012;10:735-742.
7. Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci. 2012;13:701-712.
8. Dinan TG, Cryan JF. Regulation of the stress response by the gut microbiota: implications for psychoneuroendocrinology. Psychoneuroendocrinology. 2012;37:1369-1378.
9. Foster JA, McVey Neufeld KA. Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci. 2013;36:305-312.
10. Sampson TR, Mazmanian SK. Control of brain development, function, and behavior by the microbiome. Cell Host Microbe. 2015;17:565-576.
11. Mayer EA. The neurobiology of stress and gastrointestinal disease. Gut. 2000;47:861-869.
12. Bercik P. The microbiota-gut-brain axis: learning from intestinal bacteria? Gut. 2011;60:288-289.
13. Cryan JF, O'Mahony SM. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil. 2011;23:187-192.
14. Sherwin E, Sandhu KV, Dinan TG, et al. May the force be with you: the light and dark sides of the microbiota-gut-brain axis in neuropsychiatry. CNS Drugs. 2016;30:1019-1041.
15. Dinan TG, Cryan JF. Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration. J Physiol. 2017;595:489-503.
16. Clarke G, Stilling RM, Kennedy PJ, et al. Minireview: gut microbiota: the neglected endocrine organ. Mol Endocrinol. 2014;28:1221-1238.
17. El Aidy S, Dinan TG, Cryan JF. Gut microbiota: the conductor in the orchestra of immune-neuroendocrine communication. Clin Ther. 2015;37:954-967.
18. Mayer EA, Tillisch K, Gupta A. Gut/brain axis and the microbiota. J Clin Invest. 2015;125:926-938.
19. Lyte M, Li W, Opitz N, et al. Induction of anxiety-like behavior in mice during the initial stages of infection with the agent of murine colonic hyperplasia Citrobacter rodentium. Physiol Behav. 2006;89:350-357.
20. Shanahan F. The host-microbe interface within the gut. Best Pract Res Clin Gastroenterol. 2002;16:915-931.
21. Macpherson AJ, Harris NL. Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol. 2004;4:478-485.
22. Lyte M. Microbial endocrinology in the microbiome-gut-brain axis: how bacterial production and utilization of neurochemicals influence behavior. PLoS Pathog. 2013;9:e1003726. doi: 10.1371/journal.ppat.1003726.
23. Barrett E, Ross RP, O'Toole PW, et al. c-Aminobutyric acid production by culturable bacteria from the human intestine. J Appl Microbiol. 2012;113:411-417.
24. Ross RP, Mills S, Hill C, et al. Specific metabolite production by gut microbiota as a basis for probiotic function. Int Dairy J. 2010;20:269-276.
25. O'Mahony SM, Clarke G, Borre YE, et al. Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav Brain Res. 2015;277:32-48.
26. Kennedy PJ, Cryan JF, Dinan TG, et al. Kynurenine pathway metabolism and the microbiota-gut-brain axis. Neuropharmacology. 2017;112:399-412.
27. Sudo N, Chida Y, Aiba Y, et al. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol. 2004;558:263-275.
28. Bravo JA, Forsythe P, Chew MV, et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A. 2011;108:16050-16055.
29. Neufeld KM, Kang N, Bienenstock J, et al. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol Motil. 2011;23:255-265.
30. Clarke G, Grenham S, Scully P, et al. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry. 2013;18:666-673.
31. Furness JB. The organisation of the autonomic nervous system: peripheral connections. Auton Neurosci. 2006;130:1-5.
32. Blackshaw LA, Brookes SJH, Grundy D, et al. Sensory transmission in the gastrointestinal tract. Neurogastroenterol Motil. 2007;19:1-19.
33. Bercik P, Park AJ, Sinclair D, et al. The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication. Neurogastroenterol Motil. 2011;23:1132-1139.
34. Bercik P, Verdu EF, Foster JA, et al. Chronic gastrointestinal inflammation induces anxiety-like behavior and alters central nervous system biochemistry in mice. Gastroenterology. 2010;139:2102-2112.
35. Bercik P, Denou E, Collins J, et al. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology. 2011;141:599-609, e3.
36. Kunze WA, Mao Y, Wang B, et al. Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium-dependent potassium channel opening. J Cell Mol Med. 2009;13:2261-2270.
37. Mcvey Neufeld KA, Mao YK, Bienenstock J, et al. The microbiome is essential for normal gut intrinsic primary afferent neuron excitability in the mouse. Neurogastroenterol Motil. 2013;25:e183-e188.
38. Dogra S, Sakwinska O, Soh SE, et al. Rate of establishing the gut microbiota in infancy has consequences for future health. Gut Microbes. 2015;6:321-325.
39. Goedert JJ, Hua X, Yu G, et al. 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.
40. Lax S, Smith DP, Hampton-Marcell J, et al. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science. 2014;345:1048-1052.
41. Mueller N T, Whyatt R, Hoepner L, et al. Prenatal exposure to antibiotics, cesarean section and risk of childhood obesity. Int J Obes (Lond). 2015;39:665-670.
42. Metsl J, Lundqvist A, Virta LJ, et al. Prenatal and post-natal exposure to antibiotics and risk of asthma in childhood. Clin Exp Allergy. 2015;45:137-145.
43. Borre YE, O'Keeffe GW, Clarke G, et al. Microbiota and neurodevelopmental windows: implications for brain disorders. Trends Mol Med. 2014;20:509-518.
44. 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.
45. Heijtz RD, Wang S, Anuar F, et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A. 2011;108:3047-3052.
46. Erny D, Hrabě de Angelis AL, Jaitin D, et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci. 2015;18:965-977.
47. Stilling RM, Ryan FJ, Hoban AE, et al. Microbes and neurodevelopment-absence of microbiota during early life increases activity-related transcriptional pathways in the amygdala. Brain Behav Immun. 2015;50:209-220.
48. Desbonnet L, Clarke G, Shanahan F, et al. Microbiota is essential for social development in the mouse. Mol Psychiatry. 2014;19:146-148.
49. Rager G. Systems-matching by degeneration. II. Interpretation of the generation and degeneration of retinal ganglion cells in the chicken by a mathematical model. Exp Brain Res. 1978;33:79-90.
50. Herrup K, Sunter K. Numerical matching during cerebellar development: quantitative analysis of granule cell death in staggerer mouse chimeras. J Neurosci. 1987;7:829-836.
51. Wopereis H, Oozeer R, Knipping K, et al. The first thousand days-intestinal microbiology of early life: establishing a symbiosis. Pediatr Allergy Immunol. 2014;25:428-438.
52. Ben-Ari Y. Neuropaediatric and neuroarchaeology: understanding development to correct brain disorders. Acta Paediatr. 2013;102:331-334.
53. Rapoport JL, Giedd JN, Gogtay N. Neurodevelopmental model of schizophrenia: update 2012. Mol Psychiatry. 2012;17:1228-1238.
54. Thompson BL, Levitt P, Stanwood GD. Prenatal exposure to drugs: effects on brain development and implications for policy and education. Nat Rev Neurosci. 2009;10:303-312.
55. Workman AD, Charvet CJ, Clancy B, et al. Modeling transformations of neurodevelopmental sequences across mammalian species. J Neurosci. 2013;33:7368-7383.
56. Braniste V, Al-Asmakh M, Kowal C, et al. The gut microbiota influences bloodbrain barrier permeability in mice. Sci Transl Med. 2014;6:263ra158. doi: 10.1126/ scitranslmed.3009759.
57. Engelhardt B. Development of the blood-brain barrier. Cell Tissue Res. 2003;314:119-129.
58. Hensch TK. Critical period regulation. Annu Rev Neurosci. 2004;27:549-579.
59. Knudsen EI. Sensitive periods in the development of the brain and behavior. J Cogn Neurosci. 2004;16:1412-1425.
60. Stolp HB, Liddelow SA, Śa-Pereira I, et al. Immune responses at brain barriers and implications for brain development and neurological function in later life. Front Integr Neurosci. 2013;7:61. doi: 10.3389/fnint.2013.00061.
61. Prenderville JA, Kennedy PJ, Dinan TG, et al. Adding fuel to the fire: the impact of stress on the ageing brain. Trends Neurosci. 2015;38:13-25.
62. Ogbonnaya ES, Clarke G, Shanahan F, et al. Adult hippocampal neurogenesis is regulated by the microbiome. Biol Psychiatry. 2015;78:e7-e9.
63. Knol J, Scholtens P, Kafka C, et al. Colon microflora in infants fed formula with galacto- and fructo-oligosaccharides: more like breast-fed infants. J Pediatr Gastroenterol Nutr. 2005;40:36-42.
64. 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.
65. World Health Organization. WHO statement on caesarean section rates. Reprod Health Matters. 2015;23:149-150.
66. World Health Organization. Appropriate technology for birth. Lancet. 1985;2:436-437.
67. OECD Health Data. Health at a Glance 2011: OECD Indicators. http://dx.doi.org/ 10.1787/888932524906. Published 2011:95-97. Accessed December 1, 2016.
68. Betrán AP, Merialdi M, Lauer JA, et al. Rates of caesarean section: analysis of global, regional and national estimates. Paediatr Perinat Epidemiol. 2007;21:98-113.
69. Ye J, Betrán AP, Guerrero Vela M, et al. Searching for the optimal rate of medically necessary cesarean delivery. Birth. 2014;41:237-244.
70. Ronsmans C, Holtz S, Stanton C. Socioeconomic differentials in caesarean rates in developing countries: a retrospective analysis. Lancet. 2006;368:1516-1523.
71. Lumbiganon P, Laopaiboon M, Gülmezoglu AM, et al. Method of delivery and pregnancy outcomes in Asia: the WHO global survey on maternal and perinatal health 2007-08. Lancet. 2010;375:490-499.
72. Watanabe S, Narisawa Y, Arase S, et al. Differences in fecal microflora between patients with atopic dermatitis and healthy control subjects. J Allergy Clin Immunol. 2003;111:587-591.
73. Negele K, Heinrich J, Borte M, et al. Mode of delivery and development of atopic disease during the first 2 years of life. Pediatr Allergy Immunol. 2004;15:48-54.
74. Kalliomaki M, Collado MC, Salminen S, et al. Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr. 2008;87:534-538.
75. Pandey PK, Verma P, Kumar H, et al. Comparative analysis of fecal microflora of healthy full-term Indian infants born with different methods of delivery (vaginal vs cesarean): Acinetobacter sp. prevalence in vaginally born infants. J Biosci. 2012;37:989-998.
76. Marild 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, e3.
77. Xu B, Pekkanen J, Hartikainen AL, et al. Caesarean section and risk of asthma and allergy in adulthood. J Allergy Clin Immunol. 2001;107:732-733.
78. Kero J, Gissler M, Gronlund MM, et al. Mode of delivery and asthma-is there a connection? Pediatr Res. 2002;52:6-11.
79. Algert CS, McElduff A, Morris JM, et al. Perinatal risk factors for early onset of Type 1 diabetes in a 2000-2005 birth cohort. Diabet Med. 2009;26:1193-1197.
80. Huh S Y, Rifas-Shiman S L, 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.
81. Blustein J, Attina T, Liu M, et al. Association of caesarean delivery with child adiposity from age 6 weeks to 15 years. Int J Obes (Lond). 2013;37:900-906.
82. Bisgaard H, Li N, Bonnelykke K, et al. 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-e5.
83. Roduit C, Scholtens S, de Jongste JC, et al. Asthma at 8 years of age in children born by caesarean section. Thorax. 2009;64:107-113.
84. von Mutius E. Allergies, infections and the hygiene hypothesis-the epidemiological evidence. Immunobiology. 2007;212:433-439.
85. Cardwell CR, Stene LC, Joner G, et al. Caesarean section is associated with an increased risk of childhood-onset type 1 diabetes mellitus: a meta-analysis of observational studies. Diabetologia. 2008;51:726-735.
86. Aumeunier A, Grela F, Ramadan A, et al. Systemic Toll-like receptor stimulation suppresses experimental allergic asthma and autoimmune diabetes in NOD mice. PLoS One. 2010;5:e11484. doi: 10.1371/journal.pone.0011484.
87. Mezoff EA, Aly H. The winding road to understanding the neonatal origins of inflammatory gastrointestinal disorders. J Pediatr Gastroenterol Nutr. 2013;57:543-549.
88. Akobeng AK, Ramanan AV, Buchan I, et al. Effect of breast feeding on risk of celiac disease: a systematic review and meta-analysis of observational studies. Arch Dis Child. 2006;91:39-43.
89. Jakobsson HE, Abrahamsson TR, Jenmalm MC, et al. Decreased gut microbiota diversity, delayed Bacteroidetes colonization and reduced Th1 responses in infants delivered by caesarean section. Gut. 2014;63:559-566.
90. Hansen CH, Andersen LS, Krych L, et al. Mode of delivery shapes gut colonization pattern and modulates regulatory immunity in mice. J Immunol. 2014;193:1213-1222.
91. Sevelsted A, Stokholm J, Bønnelykke K, et al. Cesarean section and chronic immune disorders. Pediatrics. 2015;135:e92-e98.
92. Li Y, Tian Y, Zhu W, et al. Cesarean delivery and risk of inflammatory bowel disease: a systematic review and meta-analysis. Scand J Gastroenterol. 2014;49:834-844.
93. Chudal R, Sourander A, Polo-Kantola P, et al. Perinatal factors and the risk of bipolar disorder in Finland. J Affect Disord. 2014;155:75-80.
94. Curran EA, O'Neill SM, Cryan JF, et al. Research review: birth by caesarean section and development of autism spectrum disorder and attention-deficit/ hyperactivity disorder: a systematic review and meta-analysis. J Child Psychol Psychiatry. 2015;56:500-508.
95. Curran EA, Cryan JF, Kenny LC, et al. Obstetrical mode of delivery and childhood behavior and psychological development in a British cohort. J Autism Dev Disord. 2016;46:603-614.
96. O'Neill SM, Curran EA, Dalman C, et al. Birth by caesarean section and the risk of adult psychosis: a population-based cohort study. Schizophr Bull. 2016;42:633-641.
97. Brander G, Rydell M, Kuja-Halkola R, et al. Association of perinatal risk factors with obsessive-compulsive disorder: a population-based birth cohort, sibling control study. JAMA Psychiatry. 2016;73:1135-1144.
98. Neufeld K-AM, Luczynski P, Dinan TG, et al. Reframing the teenage wasteland: adolescent microbiota-gut-brain axis. Can J Psychiatry. 2016;61:214-221.
99. Jost T, Lacroix C, Braegger CP, et al. New insights in gut microbiota establishment in healthy breast fed neonates. PLoS One. 2012;7:e44595. doi: 10.1371/ journal.pone.0044595.
100. 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.
101. Dominguez-Bello MG, De Jesus-Laboy KM, Shen N, et al. Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat Med. 2016;22:250-253.
102. Cunnington AJ, Sim K, Deierl A, et al. "Vaginal seeding" of infants born by caesarean section. BMJ. 2016;352:i227. doi: 10.1136/bmj.i227.
103. Yancey MK, Schuchat A, Brown LK, et al. The accuracy of late antenatal screening cultures in predicting genital group B streptococcal colonization at delivery. Obstet Gynecol. 1996;88:811-815.
104. Campbell JR, Hillier SL, Krohn MA, et al. Group B streptococcal colonization and serotype-specific immunity in pregnant women at delivery. Obstet Gynecol. 2000;96:498-503.
105. Knight R, Gilbert JA. Opinion: a mother's microbes. The Scientist. 2016. http:// mobile.the-scientist.com/article/45505/opinion-a-mother-s-microbes. Accessed December 1, 2016.
106. Money DM, Dobson S. The prevention of early-onset neonatal group B streptococcal disease. J Obstet Gynaecol Can. 2004;26:826-840.
107. Verani JR, McGee L, Schrag SJ. Prevention of perinatal group B streptococcal disease: revised guidelines from CDC, 2010. MMWR RecommRep. 2010;59:1-36.
108. UK National Screening Committee. The UK NSC policy on group B streptococcus screening in pregnancy. 2012. https://legacyscreening.phe.org.uk/ groupbstreptococcus. Accessed December 1, 2016.
109. Rook GA. Regulation of the immune system by biodiversity from the natural environment: an ecosystem service essential to health. Proc Natl Acad Sci U S A. 2013;110:18360-18367.
110. Renfrew MJ, McFadden A, Bastos MH, et al. Midwifery and quality care: findings from a new evidence-informed framework for maternal and newborn care. Lancet. 2014;384:1129-1145.
111. Collado MC, Rautava S, Aakko J, et al. Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Sci Rep. 2016;6:doi:10.1038/srep23129.
112. 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.
113. Gueimonde M, Sakata S, Kalliomaki M, et al. Effect of maternal consumption of lactobacillus GG on transfer and establishment of fecal bifidobacterial microbiota in neonates. J Pediatr Gastroenterol Nutr. 2006;42:166-170.
114. Schultz M, Gottl C, Young RJ, et al. Administration of oral probiotic bacteria to pregnant women causes temporary infantile colonization. J Pediatr Gastroenterol Nutr. 2004;38:293-297.
115. Ismail IH, Oppedisano F, Joseph SJ, et al. Prenatal administration of Lactobacillus rhamnosus has no effect on the diversity of the early infant gut microbiota. Pediatr Allergy Immunol. 2012;23:255-258.
116. Anderson S. Probiotics for preterm infants: a premature or overdue necrotizing enterocolitis prevention strategy? Neonatal Netw. 2015;34:83-101.
117. Abdulkadir B, Nelson A, Skeath T, et al. Routine use of probiotics in preterm infants: longitudinal impact on the microbiome and metabolome. Neonatology. 2016;109:239-247.
118. Lin C S, Chang C J, Lu CC, et al. Impact of the gut microbiota, prebiotics, and probiotics on human health and disease. Biomed J. 2014;37:259-268.
119. Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995;125:1401-1412.
120. Gibson GR, Probert HM, Van Loo J, et al. Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev.2004;17:259-275.
121. Delzenne NM, Neyrinck AM, Cani PD. Gut microbiota and metabolic disorders: how prebiotic can work? Br J Nutr. 2013;109:S81-S85.
122. Marques TM, Cryan JF, Shanahan F, et al. Gut microbiota modulation and implications for host health: dietary strategies to influence the gut-brain axis. Innov Food Sci Emerg Technol. 2014;22:239-247.
123. Rastall RA, Gibson GR. Recent developments in prebiotics to selectively impact beneficial microbes and promote intestinal health. Curr Opin Biotechnol. 2015;32:42-46.
124. Slavin J. Fiber and prebiotics: mechanisms and health benefits. Nutrients. 2013;5:1417-1435.
125. Fujiwara R, Takemura N, Watanabe J, et al. Maternal consumption of fructooligosaccharide diminishes the severity of skin inflammation in offspring of NC/ Nga mice. Br J Nutr. 2010;103:530-538.
126. Desbuards N, Gourbeyre P, Haure-Mirande V, et al. Impact of perinatal prebiotic consumption on gestating mice and their offspring: a preliminary report. Br J Nutr. 2012;107:1245-1248.
127. Wang M, Radlowski EC, Monaco MH, et al. Mode of delivery and early nutrition modulate microbial colonization and fermentation products in neonatal piglets. J Nutr. 2013;143:795-803.
128. Partty A, Luoto R, Kalliomaki M, et al. Effects of early prebiotic and probiotic supplementation on development of gut microbiota and fussing and crying in preterm infants: a randomized, double-blind, placebo-controlled trial. J Pediatr. 2013;163:1272-1277, e1-e2.
129. Barrett E, Deshpandey AK, Ryan CA, et al. The neonatal gut harbours distinct bifidobacterial strains. Arch Dis Child Fetal Neonatal Ed. 2015;100:F405-F410.
130. Arslanoglu S, Moro GE, Schmitt J, et al. 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.
131. Grüber C, van Stuijvenberg M, Mosca F, et al. Reduced occurrence of early atopic dermatitis because of immunoactive prebiotics among low-atopy-risk infants. J Allergy Clin Immunol. 2010;126:791-797.
132. Haarman M, Knol J. Quantitative real-time PCR assays to identify and quantify fecal Bifidobacterium species in infants receiving a prebiotic infant formula. Appl Environ Microbiol. 2005;71:2318-2324.
133. Luoto R, Ruuskanen O, Waris M, et al. Prebiotic and probiotic supplementation prevents rhinovirus infections in preterm infants: a randomized, placebocontrolled trial. J Allergy Clin Immunol. 2014;133:405-413.
134. Chua MC, Chew C, Goh A, et al. A synbiotic mixture of scGOS/lcFOS and Bifidobacterium breve M-16V is able to restore the delayed colonization of Bifidobacteria ssp. in C-section delivered infants. J Pediatric Neonatal Individualized Med. 2015;4:e040210.
135. Schouten B, van Esch BC, Hofman GA, et al. Cow milk allergy symptoms are reduced in mice fed dietary synbiotics during oral sensitization with whey. J Nutr. 2009;139:1398-1403.
136. Passeron T, Lacour JP, Fontas E, et al. Prebiotics and synbiotics: two promising approaches for the treatment of atopic dermatitis in children above 2 years. Allergy. 2006;61:431-437.
137. Nikniaz L, Mahdavi R, Ostadrahimi A, et al. Effects of synbiotic supplementation on total antioxidant capacity of human breastmilk. Breastfeed Med. 2013;8:217-222.
138. Ostadrahimi A, Nikniaz L, Mahdavi R, et al. Effects of synbiotic supplementation on lactating mothers' energy intake and BMI, and infants' growth. Int J Food Sci Nutr. 2013;64:711-714.
139. Hinde K, German JB. Food in an evolutionary context: insights from mother's milk. J Sci Food Agric. 2012;92:2219-2223.
140. Hinde K, Lewis ZT. Mother's littlest helpers. Science. 2015;348:1427-1428.
141. Murphy K, Curley D, Callaghan T, et al. The composition of human milk and infant faecal microbiota over first three months of life. Sci Rep. 2017;7:40597. doi: 10.1038/srep40597.
142. Bode L. Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology. 2012;22:1147-1162.
143. Sela DA, Chapman J, Adeuya A, et al. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci U S A. 2008;105:18964-18969.
144. Huda MN, Lewis Z, Kalanetra KM, et al. Stool microbiota and vaccine responses of infants. Pediatrics. 2014;134:e362-e372.
145. Houghteling PD, Walker WA. Why is initial bacterial colonization of the intestine important to infants' and children's health? J Pediatr Gastroenterol Nutr. 2015;60:294-307.
146. Bode L. Human milk oligosaccharides: prebiotics and beyond. Nutr Rev. 2009;67:S183-S191.
147. Ding T, Schloss PD. Dynamics and associations of microbial community types across the human body. Nature. 2014;509:357-360.
148. Schwartz S, Friedberg I, Ivanov IV, et al. A metagenomic study of diet-dependent interaction between gut microbiota and host in infants reveals differences in immune response. Genome Biol. 2012;13:doi: 10.1186/gb-2012-13-4-r32.
149. McGuire MK, McGuire MA. Human milk: mother nature's prototypical probiotic food? Adv Nutr. 2015;6:112-123.
150. Ardeshir A, Narayan NR, Mendez-Lagares G, et al. Breast-fed and bottle-fed infant rhesus macaques develop distinct gut microbiotas and immune systems. Sci Transl Med. 2014;6:doi: 10.1126/scitranslmed.3008791.
151. Hu Y, Yang X, Qin J, et al. Metagenome-wide analysis of antibiotic resistance genes in a large cohort of human gut microbiota. Nat Commun. 2013;4:2151.
152. Prior E, Santhakumaran S, Gale C, et al. Breastfeeding after cesarean delivery: a systematic review and meta-analysis of world literature. Am J Clin Nutr. 2012;95:1113-1135.
153. Miyata J, Arita M. Role of omega-3 fatty acids and their metabolites in asthma and allergic diseases. Allergol Int. 2015;64:27-34.
154. Yates CM, Calder PC, Ed Rainger G. Pharmacology and therapeutics of omega-3 polyunsaturated fatty acids in chronic inflammatory disease. Pharmacol Ther.2014;141:272-282.
155. Pusceddu MM, El Aidy S, Crispie F, et al. N-3 polyunsaturated fatty acids (PUFAs) reverse the impact of early-life stress on the gut microbiota. PLoS One. 2015;10:e0142228.
156. Miles, E.A, Calder, PC. Omega-6 and omega-3 polyunsaturated fatty acids and allergic diseases in infancy and childhood. Curr Pharm Des. 2014;20:946-953.
157. Melody M, Vincent R, Mori TA, et al. Effects of omega-3 and omega-6 fatty acids on human placental cytokine production. Placenta. 2015;36:34-40.
158. Hsieh AT, Brenna JT. Dietary docosahexaenoic acid but not arachidonic acid influences central nervous system fatty acid status in baboon neonates. Prostaglandins Leukot Essent Fatty Acids. 2009;81:105-110.
159. Stevens J, Keim SA. How research on charitable giving can inform strategies to promote human milk donations to milk banks. J Hum Lact. 2015;31:344-347.
160. Cabrera-Rubio R, Mira-Pascual L, Mira A, et al. Impact of mode of delivery on the milk microbiota composition of healthy women. J Dev Orig Health Dis. 2016;7:54-60.
161. Rodkiewicz B, Hardell LI, Pawlikowska-Rojewska B, et al. Fatty acid composition of human breast milk. Changes during the first week after delivery. Ups J Med Sci. 1981;86:279-289.
162. Sundekilde UK, Downey E, O'Mahony JA, et al. The effect of gestational and lactational age on the human milk metabolome. Nutrients. 2016;8:doi: 10.3390/ nu8050304.
163. MacKenzie C, Javanparast S, Newman L. Mothers' knowledge of and attitudes towards human milk banking in South Australia: a qualitative analysis. J Hum Lact. 2013;29:222-229.
164. Betran AP, Torloni MR, Zhang JJ, et al. WHO Statement on caesarean section rates. BJOG. 2016;123:667-670.
165. Ahmed S, Tunçalp O. Burden of obstetric fistula: from measurement to action. Lancet Glob Health. 2015;3:e243-e244.
166. Black M, Bhattacharya S, Philip S, et al. Planned cesarean delivery at termand adverse outcomes in childhood health. JAMA. 2015;314:2271-2279.
167. Mazzola G, Murphy K, Ross RP, et al. Early gut microbiota perturbations following intrapartum antibiotic prophylaxis to prevent group B Streptococcal disease. PLoS One. 2016;11:doi: 10.1371/journal.pone.0157527.
168. Jašarević E, Rodgers AB, Bale TL. A novel role for maternal stress and microbial transmission in early life programming and neurodevelopment. Neurobiol Stress. 2015;1:81-88.
169. Jašarević E, Howerton CL, Howard CD, et al. Alterations in the vaginal microbiome by maternal stress are associated with metabolic reprogramming of the offspring gut and brain. Endocrinology. 2015;156:3265-3276.
170. Rasmussen SA, Chu SY, Kim SY, et al. Maternal obesity and risk of neural tube defects: a metaanalysis. Am J Obstet Gynecol. 2008;198:611-619.
171. Papachatzi E, Dimitriou G, Dimitropoulos K, et al. Prepregnancy obesity: maternal, neonatal and childhood outcomes. J Neonatal Perinatal Med. 2013;6:203-216.
172. Gaudet L, Ferraro ZM, Wen SW, et al. Maternal obesity and occurrence of fetal macrosomia: a systematic review and meta-analysis. Biomed Res Int. 2014;2014:doi: 10.1155/2014/640291.
173. Lucas A. Programming by early nutrition: an experimental approach. J Nutr. 1998;128:401S-406S.
174. Mueller NT, Bakacs E, Combellick J, et al. The infant microbiome development: mom matters. Trends Mol Med. 2015;21:109-117.
175. Kelly JR, Borre Y, O'Brien C, et al. Transferring the blues: depression-associated gut microbiota induces neurobehavioural changes in the rat. J Psychiatr Res. 2016;82:109-118.
176. Hoban AE, Stilling RM, Ryan FJ, et al. Regulation of prefrontal cortex myelination by the microbiota. Transl Psychiatry. 2016;6:doi: 10.1038/ tp.2016.42.
177. Luczynski P, Whelan SO, O'Sullivan C, et al. Adult microbiota-deficient mice have distinct dendritic morphological changes: differential effects in the amygdala and hippocampus. Eur J Neurosci. 2016;44:2654-2666.
178. Dinan TG, Stanton C, Cryan JF. Psychobiotics: a novel class of psychotropic. Biol Psychiatry. 2013;74:720-726.
179. Allen AP, Hutch W, Borre Y, et al. Bifidobacterium longum 1714 as a translational psychobiotic: modulation of stress, electrophysiology and neurocognition in healthy volunteers. Translational Psychiatry 2016;6:doi: 10.1038/ tp.2016.191.
180. Hill CJ, Lynch DB, Murphy K, et al. Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort. Microbiome. 2017;5:4.