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Abstract

The prenatal and early postnatal periods are stages during which dynamic changes and the development of the brain and gut microbiota occur, and nutrition is one of the most important modifiable factors that influences this process. Given the bidirectional cross talk between the gut microbiota and the brain through the microbiota–gut–brain axis (MGBA), there is growing interest in evaluating the potential effects of nutritional interventions administered during these critical developmental windows on gut microbiota composition and function and their association with neurodevelopmental outcomes. We review recent preclinical and clinical evidence from animal studies and infant/child populations. Although further research is needed, growing evidence suggests that different functional nutrients affect the establishment and development of the microbiota–gut–brain axis and could have preventive and therapeutic use in the treatment of neuropsychiatric disorders. Therefore, more in-depth knowledge regarding the effect of nutrition on the MGBA during critical developmental windows may enable the prevention of later neurocognitive and behavioral disorders and allow the establishment of individualized nutrition-based programs that can be used from the prenatal to the early and middle stages of life.

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2023-08-21
2024-04-29
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Literature Cited

  1. 1.
    Adıgüzel E, Çiçek B, Ünal G, Aydın MF, Barlak-Keti D. 2022. Probiotics and prebiotics alleviate behavioral deficits, inflammatory response, and gut dysbiosis in prenatal VPA-induced rodent model of autism. Physiol. Behav. 256:113961
    [Google Scholar]
  2. 2.
    Afroz KF, Reyes N, Young K, Parikh K, Misra V, Alviña K. 2021. Altered gut microbiome and autism like behavior are associated with parental high salt diet in male mice. Sci. Rep. 11:8364
    [Google Scholar]
  3. 3.
    Ainonen S, Tejesvi MV, Mahmud M, Paalanne N, Pokka T et al. 2022. Antibiotics at birth and later antibiotic courses: effects on gut microbiota. Pediatr. Res. 91:1154–62
    [Google Scholar]
  4. 4.
    Arslanova A, Tarasova A, Alexandrova A, Novoselova V, Shaidullov I et al. 2021. Protective effects of probiotics on cognitive and motor functions, anxiety level, visceral sensitivity, oxidative stress and microbiota in mice with antibiotic-induced dysbiosis. Life 11:8764
    [Google Scholar]
  5. 5.
    Azad MB, Konya T, Maughan H, Guttman DS, Field CJ et al. 2013. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. Can. Med. Assoc. J. 185:5385–94
    [Google Scholar]
  6. 6.
    Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H et al. 2015. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17:5690–703
    [Google Scholar]
  7. 7.
    Barrett HL, Gomez-Arango LF, Wilkinson SA, McIntyre HD, Callaway LK et al. 2018. A vegetarian diet is a major determinant of gut microbiota composition in early pregnancy. Nutrients 10:7890
    [Google Scholar]
  8. 8.
    Bellaiche M, Ludwig T, Arciszewska M, Bongers A, Gomes C et al. 2021. Safety and tolerance of a novel anti-regurgitation formula: a double-blind, randomized, controlled trial. J. Pediatr. Gastroenterol. Nutr. 73:5579–85
    [Google Scholar]
  9. 9.
    Bercik P, Denou E, Collins J, Jackson W, Lu J et al. 2011. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 141:2599–609
    [Google Scholar]
  10. 10.
    Berding K, Wang M, Monaco MH, Alexander LS, Mudd AT et al. 2016. Prebiotics and bioactive milk fractions affect gut development, microbiota, and neurotransmitter expression in piglets. J. Pediatr. Gastroenterol. Nutr. 63:6688–97
    [Google Scholar]
  11. 11.
    Boehm G, Lidestri M, Casetta P, Jelinek J, Negretti F et al. 2002. Supplementation of a bovine milk formula with an oligosaccharide mixture increases counts of faecal bifidobacteria in preterm infants. Arch. Dis. Child. Fetal Neonatal Ed. 86:3F178–81
    [Google Scholar]
  12. 12.
    Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM et al. 2011. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. PNAS 108:3816050–55
    [Google Scholar]
  13. 13.
    Brink LR, Lönnerdal B. 2020. Milk fat globule membrane: the role of its various components in infant health and development. J. Nutr. Biochem. 85:108465
    [Google Scholar]
  14. 14.
    Brown AS, Begg MD, Gravenstein S, Schaefer CA, Wyatt RJ et al. 2004. Serologic evidence of prenatal influenza in the etiology of schizophrenia. Arch. Gen. Psychiatry 61:8774–80
    [Google Scholar]
  15. 15.
    Buffington SA, Di Prisco GV, Auchtung TA, Ajami NJ, Petrosino JF, Costa-Mattioli M. 2016. Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell 165:71762–75
    [Google Scholar]
  16. 16.
    Calatayud M, Koren O, Collado MC. 2019. Maternal microbiome and metabolic health program microbiome development and health of the offspring. Trends Endocrinol. Metab. 30:10735–44
    [Google Scholar]
  17. 17.
    Carabotti M, Scirocco A, Maselli MA, Severi C. 2015. The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann. Gastroenterol. Q. 28:2203–9
    [Google Scholar]
  18. 18.
    Casas M, Forns J, Martínez D, Guxens M, Fernandez-Somoano A et al. 2017. Maternal pre-pregnancy obesity and neuropsychological development in pre-school children: a prospective cohort study. Pediatr. Res. 82:4596–606
    [Google Scholar]
  19. 19.
    Cerdó T, Ruíz A, Acuña I, Nieto-Ruiz A, Diéguez E et al. 2022. A synbiotics, long chain polyunsaturated fatty acids, and milk fat globule membranes supplemented formula modulates microbiota maturation and neurodevelopment. Clin. Nutr. 41:81697–711
    [Google Scholar]
  20. 20.
    Cetin I, Bühling K, Demir C, Kortam A, Prescott SL et al. 2019. Impact of micronutrient status during pregnancy on early nutrition programming. Ann. Nutr. Metab. 74:4269–78
    [Google Scholar]
  21. 21.
    Chakrabarti A, Geurts L, Hoyles L, Iozzo P, Kraneveld AD et al. 2022. The microbiota–gut–brain axis: pathways to better brain health. Perspectives on what we know, what we need to investigate and how to put knowledge into practice. Cell Mol. Life Sci. 79:280
    [Google Scholar]
  22. 22.
    Chooi YC, Ding C, Magkos F. 2019. The epidemiology of obesity. Metabolism 92:6–10
    [Google Scholar]
  23. 23.
    Chu DM, Ma J, Prince AL, Antony KM, Seferovic MD, Aagaard KM. 2017. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat. Med. 23:3314–26
    [Google Scholar]
  24. 24.
    Chua MC, Ben-Amor K, Lay C, Neo AGE, Chiang WC et al. 2017. Effect of synbiotic on the gut microbiota of cesarean delivered infants: a randomized, double-blind, multicenter study. J. Pediatr. Gastroenterol. Nutr. 65:1102–6
    [Google Scholar]
  25. 25.
    Codagnone MG, Stanton C, O'Mahony SM, Dinan TG, Cryan JF 2019. Microbiota and neurodevelopmental trajectories: role of maternal and early-life nutrition. Ann. Nutr. Metab. 74:216–27
    [Google Scholar]
  26. 26.
    Collado MC, Isolauri E, Laitinen K, Salminen S. 2010. Effect of mother's weight on infant's microbiota acquisition, composition, and activity during early infancy: a prospective follow-up study initiated in early pregnancy. Am. J. Clin. Nutr. 92:51023–30
    [Google Scholar]
  27. 27.
    Collado MC, Vinderola G, Salminen S. 2019. Postbiotics: facts and open questions. A position paper on the need for a consensus definition. Benef. Microbes 10:7711–19
    [Google Scholar]
  28. 28.
    Collins J, Borojevic R, Verdu EF, Huizinga JD, Ratcliffe EM. 2014. Intestinal microbiota influence the early postnatal development of the enteric nervous system. Neurogastroenterol. Motil. 26:198–107
    [Google Scholar]
  29. 29.
    Collins JM, Caputi V, Manurung S, Gross G, Fitzgerald P et al. 2022. Supplementation with milk fat globule membrane from early life reduces maternal separation–induced visceral pain independent of enteric nervous system or intestinal permeability changes in the rat. Neuropharmacology 210:109026
    [Google Scholar]
  30. 30.
    Colombo J, Carlson SE, Algarín C, Reyes S, Chichlowski M et al. 2021. Developmental effects on sleep-wake patterns in infants receiving a cow's milk–based infant formula with an added prebiotic blend: a randomized controlled trial. Pediatr. Res. 89:51222–31
    [Google Scholar]
  31. 31.
    Cryan JF, Mazmanian SK. 2022. Microbiota–brain axis: context and causality. Science 376:6596938–39
    [Google Scholar]
  32. 32.
    Cryan JF, O'Riordan KJ, Cowan CSM, Sandhu KV, Bastiaanssen TFS et al. 2019. The microbiota–gut–brain axis. Physiol. Rev. 99:41877–2013
    [Google Scholar]
  33. 33.
    Davis RL 2018. Neurodevelopment: Inflammation matters. Linking Environmental Exposure to Neurodevelopmental Disorders M Aschner, LG Costa 227–64. Amsterdam: Elsevier
    [Google Scholar]
  34. 34.
    De Almagro García MC, Moreno Muñoz JA, Jiménez López J, Rodríguez-Palmero Seuma M. 2017. New ingredients in infant formula. Health and functional benefits. Nutr. Hosp. 34:Suppl. 48–12
    [Google Scholar]
  35. 35.
    De Angelis M, Piccolo M, Vannini L, Siragusa S, De Giacomo A et al. 2013. Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified. PLOS ONE 8:10e76993
    [Google Scholar]
  36. 36.
    Deoni S, Dean D 3rd, Joelson S, O'Regan J, Schneider N. 2018. Early nutrition influences developmental myelination and cognition in infants and young children. NeuroImage 178:649–59
    [Google Scholar]
  37. 37.
    Di Gesù CM, Matz LM, Buffington SA. 2021. Diet-induced dysbiosis of the maternal gut microbiome in early life programming of neurodevelopmental disorders. Neurosci. Res. 168:3–19
    [Google Scholar]
  38. 38.
    Edlow AG. 2017. Maternal obesity and neurodevelopmental and psychiatric disorders in offspring. Prenat. Diagn. 37:195–110
    [Google Scholar]
  39. 39.
    El-Ansary A, Ben Bacha A, Bjørklund G, Al-Orf N, Bhat RS et al. 2018. Probiotic treatment reduces the autistic-like excitation/inhibition imbalance in juvenile hamsters induced by orally administered propionic acid and clindamycin. Metab. Brain Dis. 33:41155–64
    [Google Scholar]
  40. 40.
    El-Ansary A, Ben Bacha A, Bjørklund G, Al-Orf N, Bhat RS et al. 2020. Perinatal factors affect the gut microbiota up to four years after birth. Cell 12:550593
    [Google Scholar]
  41. 41.
    Erny D, Hrabě de Angelis AL, Jaitin D, Wieghofer P, Staszewski O et al. 2015. Host microbiota constantly control maturation and function of microglia in the CNS. Nat. Neurosci. 18:7965–77
    [Google Scholar]
  42. 42.
    Georgieff MK. 2007. Nutrition and the developing brain: nutrient priorities and measurement. Am. J. Clin. Nutr. 85:2S614–20
    [Google Scholar]
  43. 43.
    Gibb R, Kovalchuk A 2018. Brain development. The Neurobiology of Brain and Behavioral Development R Gibb, B Kolb 3–27. San Diego, CA: Academic
    [Google Scholar]
  44. 44.
    Grimaldi R, Gibson GR, Vulevic J, Giallourou N, Castro-Mejía JL et al. 2018. A prebiotic intervention study in children with autism spectrum disorders (ASDs). Microbiome 6:133
    [Google Scholar]
  45. 45.
    Grissom NM, George R, Reyes TM. 2017. The hypothalamic transcriptional response to stress is severely impaired in offspring exposed to adverse nutrition during gestation. Neuroscience 342:200–11
    [Google Scholar]
  46. 46.
    Guidetti C, Salvini E, Viri M, Deidda F, Amoruso A et al. 2022. Randomized double-blind crossover study for evaluating a probiotic mixture on gastrointestinal and behavioral symptoms of autistic children. J. Clin. Med. 11:185263
    [Google Scholar]
  47. 47.
    Guo Q, Tang Y, Li Y, Xu Z, Zhang D et al. 2021. Perinatal high-salt diet induces gut microbiota dysbiosis, bile acid homeostasis disbalance, and NAFLD in weanling mice offspring. Nutrients 13:72135
    [Google Scholar]
  48. 48.
    Harmsen HJ, Wildeboer-Veloo AC, Raangs GC, Wagendorp AA, Klijn N et al. 2000. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J. Pediatr. Gastroenterol. Nutr. 30:161–67
    [Google Scholar]
  49. 49.
    Hebert JC, Radford-Smith DE, Probert F, Ilott N, Chan KW et al. 2021. Mom's diet matters: Maternal prebiotic intake in mice reduces anxiety and alters brain gene expression and the fecal microbiome in offspring. Brain. Behav. Immun. 91:230–44
    [Google Scholar]
  50. 50.
    Heijtz RD, Wang S, Anuar F, Qian Y, Björkholm B et al. 2011. Normal gut microbiota modulates brain development and behavior. PNAS 108:73047–52
    [Google Scholar]
  51. 51.
    Hill CJ, Lynch DB, Murphy K, Ulaszewska M, Jeffery IB et al. 2017. Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET cohort. Microbiome 5:4
    [Google Scholar]
  52. 52.
    Hollister EB, Riehle K, Luna RA, Weidler EM, Rubio-Gonzales M et al. 2015. Structure and function of the healthy pre-adolescent pediatric gut microbiome. Microbiome 3:36
    [Google Scholar]
  53. 53.
    Horta BL, de Sousa BA, de Mola CL. 2018. Breastfeeding and neurodevelopmental outcomes. Curr. Opin. Clin. Nutr. Metab. Care 21:3174–78
    [Google Scholar]
  54. 54.
    Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER et al. 2013. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155:71451–63
    [Google Scholar]
  55. 55.
    Hu J, Ma L, Nie Y, Chen J, Zheng W et al. 2018. A microbiota-derived bacteriocin targets the host to confer diarrhea resistance in early-weaned piglets. Cell Host Microbe 24:6817–32.e8
    [Google Scholar]
  56. 56.
    Jacobi SK, Yatsunenko T, Li D, Dasgupta S, Yu RK et al. 2016. Dietary isomers of sialyllactose increase ganglioside sialic acid concentrations in the corpus callosum and cerebellum and modulate the colonic microbiota of formula-fed piglets. J. Nutr. 146:2200–8
    [Google Scholar]
  57. 57.
    Jena A, Montoya CA, Mullaney JA, Dilger RN, Young W et al. 2020. Gut–brain axis in the early postnatal years of life: a developmental perspective. Front. Integr. Neurosci. 14:44
    [Google Scholar]
  58. 58.
    Jian C, Carpén N, Helve O, de Vos WM, Korpela K, Salonen A. 2021. Early-life gut microbiota and its connection to metabolic health in children: perspective on ecological drivers and need for quantitative approach. eBioMedicine 69:103475
    [Google Scholar]
  59. 59.
    John CC, Black MM, Nelson CA 3rd. 2017. Neurodevelopment: the impact of nutrition and inflammation during early to middle childhood in low-resource settings. Pediatrics 139:Suppl. 1S59–71
    [Google Scholar]
  60. 60.
    Johnson D, Letchumanan V, Thurairajasingam S, Lee L-H. 2020. A revolutionizing approach to autism spectrum disorder using the microbiome. Nutrients 12:71983
    [Google Scholar]
  61. 61.
    Kandeel WA, Meguid NA, Bjørklund G, Eid EM, Farid M et al. 2020. Impact of Clostridium bacteria in children with autism spectrum disorder and their anthropometric measurements. J. Mol. Neurosci. 70:6897–907
    [Google Scholar]
  62. 62.
    Kayyal M, Javkar T, Firoz Mian M, Binyamin D, Koren O et al. 2020. Sex dependent effects of post-natal penicillin on brain, behavior and immune regulation are prevented by concurrent probiotic treatment. Sci. Rep. 10:10318
    [Google Scholar]
  63. 63.
    Kong Q, Tian P, Zhao J, Zhang H, Wang G, Chen W. 2021. The autistic-like behaviors development during weaning and sexual maturation in VPA-induced autistic-like rats is accompanied by gut microbiota dysbiosis. PeerJ 3:9
    [Google Scholar]
  64. 64.
    Kong Q, Wang B, Tian P, Li X, Zhao J et al. 2021. Daily intake of Lactobacillus alleviates autistic-like behaviors by ameliorating the 5-hydroxytryptamine metabolic disorder in VPA-treated rats during weaning and sexual maturation. Food Funct. 12:62591–604
    [Google Scholar]
  65. 65.
    Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K et al. 2012. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150:3470–80
    [Google Scholar]
  66. 66.
    Latuga MS, Stuebe A, Seed PC. 2014. A review of the source and function of microbiota in breast milk. Semin. Reprod. Med. 32:168–73
    [Google Scholar]
  67. 67.
    Leclercq S, Mian FM, Stanisz AM, Bindels LB, Cambier E et al. 2017. Low-dose penicillin in early life induces long-term changes in murine gut microbiota, brain cytokines and behavior. Nat. Commun. 8:15062
    [Google Scholar]
  68. 68.
    LeCouffe NE, Westerbeek EAM, van Schie PEM, Schaaf VAM, Lafeber HN, van Elburg RM. 2014. Neurodevelopmental outcome during the first year of life in preterm infants after supplementation of a prebiotic mixture in the neonatal period: a follow-up study. Neuropediatrics 45:22–29
    [Google Scholar]
  69. 69.
    Leo A, De Caro C, Mainardi P, Tallarico M, Nesci V et al. 2021. Increased efficacy of combining prebiotic and postbiotic in mouse models relevant to autism and depression. Neuropharmacology 198:108782
    [Google Scholar]
  70. 70.
    Leyrolle Q, Decoeur F, Briere G, Amadieu C, Quadros ARA A et al. 2021. Maternal dietary omega-3 deficiency worsens the deleterious effects of prenatal inflammation on the gut-brain axis in the offspring across lifetime. Neuropsychopharmacology 46:3579–602
    [Google Scholar]
  71. 71.
    Liang W, Li H, Zhou H, Wang M, Zhao X et al. 2021. Effects of Taraxacum and Astragalus extracts combined with probiotic Bacillus subtilis and Lactobacillus on Escherichia coli–infected broiler chickens. Poult. Sci. 100:4101007
    [Google Scholar]
  72. 72.
    Lou M, Cao A, Jin C, Mi K, Xiong X et al. 2022. Deviated and early unsustainable stunted development of gut microbiota in children with autism spectrum disorder. Gut 71:81588–99
    [Google Scholar]
  73. 73.
    Maher SE, O'Brien EC, Moore RL, Byrne DF, Geraghty AA et al. 2020. The association between the maternal diet and the maternal and infant gut microbiome: a systematic review. Br. J. Nutr. 4:1–29
    [Google Scholar]
  74. 74.
    Margolis KG, Cryan JF, Mayer EA. 2021. The microbiota–gut–brain axis: from motility to mood. Gastroenterology 160:51486–501
    [Google Scholar]
  75. 75.
    Martín R, Langa S, Reviriego C, Jimínez E, Marín ML et al. 2003. Human milk is a source of lactic acid bacteria for the infant gut. J. Pediatr. 143:6754–58
    [Google Scholar]
  76. 76.
    Martinat M, Rossitto M, Di Miceli M, Layé S. 2021. Perinatal dietary polyunsaturated fatty acids in brain development, role in neurodevelopmental disorders. Nutrients 13:41185
    [Google Scholar]
  77. 77.
    Matamoros S, Gras-Leguen C, Le Vacon F, Potel G, de La Cochetiere M-F 2013. Development of intestinal microbiota in infants and its impact on health. Trends Microbiol. 21:4167–73
    [Google Scholar]
  78. 78.
    McDonald SD, Han Z, Mulla S, Beyene J. 2010. Overweight and obesity in mothers and risk of preterm birth and low birth weight infants: systematic review and meta-analyses. BMJ 341:c3428
    [Google Scholar]
  79. 79.
    McFarland LV. 2008. Antibiotic-associated diarrhea: epidemiology, trends and treatment. Future Microbiol. 3:5563–78
    [Google Scholar]
  80. 80.
    Mekonnen SA, Merenstein D, Fraser CM, Marco ML. 2020. Molecular mechanisms of probiotic prevention of antibiotic-associated diarrhea. Curr. Opin. Biotechnol. 61:226–34
    [Google Scholar]
  81. 81.
    Mesa MD, Loureiro B, Iglesia I, Fernandez Gonzalez S, Llurba Olivé E et al. 2020. The evolving microbiome from pregnancy to early infancy: a comprehensive review. Nutrients 12:1133
    [Google Scholar]
  82. 82.
    Nagashima H, Morio Y, Meshitsuka S, Yamane K, Nanjo Y, Teshima R. 2010. High-resolution nuclear magnetic resonance spectroscopic study of metabolites in the cerebrospinal fluid of patients with cervical myelopathy and lumbar radiculopathy. Eur. Spine J. 19:81363–68
    [Google Scholar]
  83. 83.
    Nagpal R, Tsuji H, Takahashi T, Nomoto K, Kawashima K et al. 2017. Ontogenesis of the gut microbiota composition in healthy, full-term, vaginally born and breast-fed infants over the first 3 years of life: a quantitative bird's-eye view. Front. Microbiol. 8:1388
    [Google Scholar]
  84. 84.
    Nakano T, Sugawara M, Kawakami H. 2001. Sialic acid in human milk: composition and functions. Acta Paediatr. Taiwan. 42:111–17
    [Google Scholar]
  85. 85.
    Naqvi S, Asar TO, Kumar V, Al-Abbasi FA, Alhayyani S et al. 2021. A cross-talk between gut microbiome, salt and hypertension. Biomed. Pharmacother. 134:111156
    [Google Scholar]
  86. 86.
    Neuman H, Koren O. 2017. The pregnancy microbiome. Intestinal Microbiome: Functional Aspects in Health and Disease1–9. Nutr. Inst. Worksh. Ser. 88. Basel, Switz.: Nestec/Karger Nestlé
    [Google Scholar]
  87. 87.
    Nuriel-Ohayon M, Neuman H, Koren O. 2016. Microbial changes during pregnancy, birth, and infancy. Front. Microbiol. 7:1031
    [Google Scholar]
  88. 88.
    O'Riordan KJ, Collins MK, Moloney GM, Knox EG, Aburto MR et al. 2022. Short chain fatty acids: microbial metabolites for gut–brain axis signalling. Mol. Cell. Endocrinol. 546:111572
    [Google Scholar]
  89. 89.
    Oliveros E, Martín M, Torres-Espínola FJ, Segura-Moreno M, Ramírez M et al. 2021. Human milk levels of 2-fucosyllactose and 6-sialyllactose are positively associated with infant neurodevelopment and are not impacted by maternal BMI or diabetic status. J. Nutr. Food Sci. 4:100024
    [Google Scholar]
  90. 90.
    Oliveros E, Ramirez M, Vazquez E, Barranco A, Gruart A et al. 2016. Oral supplementation of 2′-fucosyllactose during lactation improves memory and learning in rats. J. Nutr. Biochem. 31:20–27
    [Google Scholar]
  91. 91.
    Oliveros E, Vázquez E, Barranco A, Ramírez M, Gruart A et al. 2018. Sialic acid and sialylated oligosaccharide supplementation during lactation improves learning and memory in rats. Nutrients 10:101519
    [Google Scholar]
  92. 92.
    Padial-Jaudenes M, Castanys-Munoz E, Ramirez M, Lasekan J. 2020. Physiological impact of palm olein or palm oil in infant formulas: a review of clinical evidence. Nutrients 12:123676
    [Google Scholar]
  93. 93.
    Parenti I, Rabaneda LG, Schoen H, Novarino G. 2020. Neurodevelopmental disorders: from genetics to functional pathways. Trends Neurosci. 43:8608–21
    [Google Scholar]
  94. 94.
    Parracho HMRT, Gibson GR, Knott F, Bosscher D, Kleerebezem M, McCartney AL. 2010. A double-blind, placebo-controlled, crossover-designed probiotic feeding study in children diagnosed with autistic spectrum disorders. Int. J. Probiotics Prebiotics 5:269–74
    [Google Scholar]
  95. 95.
    Pärtty A, Kalliomäki M, Wacklin P, Salminen S, Isolauri E. 2015. A possible link between early probiotic intervention and the risk of neuropsychiatric disorders later in childhood: a randomized trial. Pediatr. Res. 77:6823–28
    [Google Scholar]
  96. 96.
    Perani CV, Neumann ID, Reber SO, Slattery DA. 2015. High-fat diet prevents adaptive peripartum-associated adrenal gland plasticity and anxiolysis. Sci. Rep. 5:14821
    [Google Scholar]
  97. 97.
    Perry RJ, Peng L, Barry NA, Cline GW, Zhang D et al. 2016. Acetate mediates a microbiome-brain-β-cell axis to promote metabolic syndrome. Nature 534:7606213–17
    [Google Scholar]
  98. 98.
    Ratsika A, Codagnone MC, O'Mahony S, Stanton C, Cryan JF 2021. Priming for life: early life nutrition and the microbiota–gut–brain axis. Nutrients 13:2423
    [Google Scholar]
  99. 99.
    Rautava S, Collado MC, Salminen S, Isolauri E. 2012. Probiotics modulate host-microbe interaction in the placenta and fetal gut: a randomized, double-blind, placebo-controlled trial. Neonatology 102:3178–84
    [Google Scholar]
  100. 100.
    Robertson RC, Oriach CS, Murphy K, Moloney GM, Cryan JF et al. 2017. Omega-3 polyunsaturated fatty acids critically regulate behaviour and gut microbiota development in adolescence and adulthood. Brain. Behav. Immun. 59:21–37
    [Google Scholar]
  101. 101.
    Rodriguez-Herrera A, Tims S, Polman J, Porcel Rubio R, Muñoz Hoyos A et al. 2022. Early-life fecal microbiome and metabolome dynamics in response to an intervention with infant formula containing specific prebiotics and postbiotics. Am. J. Physiol. Liver Physiol. 322:6G571–82
    [Google Scholar]
  102. 102.
    Romijn JA, Corssmit EP, Havekes LM, Pijl H. 2008. Gut-brain axis. Curr. Opin. Clin. Nutr. Metab. Care 11:4518–21
    [Google Scholar]
  103. 103.
    Ronald A, Pennell CE, Whitehouse AJO. 2011. Prenatal maternal stress associated with ADHD and autistic traits in early childhood. Front. Psychol. 1:223
    [Google Scholar]
  104. 104.
    Rosa R, Ornella R, Caruso Maria G, Elisa S, Maria N et al. 2018. The role of diet in the prevention and treatment of inflammatory bowel diseases. Acta Biomed. 89:Suppl. 960–75
    [Google Scholar]
  105. 105.
    Russell JT, Ruoss JL, de la Cruz D, Li N, Bazacliu C et al. 2021. Antibiotics and the developing intestinal microbiome, metabolome and inflammatory environment in a randomized trial of preterm infants. Sci. Rep. 11:1943
    [Google Scholar]
  106. 106.
    Rutsch A, Kantsjö JB, Ronchi F. 2020. The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology. Front. Immunol. 11:604179
    [Google Scholar]
  107. 107.
    Sanders RA, Crozier K. 2018. How do informal information sources influence women's decision-making for birth? A meta-synthesis of qualitative studies. BMC Pregnancy Childbirth 18:21
    [Google Scholar]
  108. 108.
    Santocchi E, Guiducci L, Fulceri F, Billeci L, Buzzigoli E et al. 2016. Gut to brain interaction in Autism Spectrum Disorders: a randomized controlled trial on the role of probiotics on clinical, biochemical and neurophysiological parameters. BMC Psychiatry 16:183
    [Google Scholar]
  109. 109.
    Santocchi E, Guiducci L, Prosperi M, Calderoni S, Gaggini M et al. 2020. Effects of probiotic supplementation on gastrointestinal, sensory and core symptoms in autism spectrum disorders: a randomized controlled trial. Front. Psychiatry 11:550593
    [Google Scholar]
  110. 110.
    Sarkar SR, Mazumder PM, Banerjee S. 2020. Probiotics protect against gut dysbiosis associated decline in learning and memory. J. Neuroimmunol. 348:577390
    [Google Scholar]
  111. 111.
    Sarkar SR, Mazumder PM, Banerjee S. 2022. Oligosaccharide and flavanoid mediated prebiotic interventions to treat gut dysbiosis associated cognitive decline. J. Neuroimmune Pharmacol. 17:1/294–110
    [Google Scholar]
  112. 112.
    Sauer PJJ. 2013. Can we define an infant's need from the composition of human milk?. Am. J. Clin. Nutr. 98:Suppl. CS521–28
    [Google Scholar]
  113. 113.
    Saunders PR, Santos J, Hanssen NPM, Yates D, Groot JA, Perdue MH. 2002. Physical and psychological stress in rats enhances colonic epithelial permeability via peripheral CRH. Dig. Dis. Sci. 47:1208–15
    [Google Scholar]
  114. 114.
    Schwartz DJ, Langdon AE, Dantas G. 2020. Understanding the impact of antibiotic perturbation on the human microbiome. Genome Med. 12:182
    [Google Scholar]
  115. 115.
    Seferovic MD, Mohammad M, Pace RM, Engevik M, Versalovic J et al. 2020. Maternal diet alters human milk oligosaccharide composition with implications for the milk metagenome. Sci. Rep. 10:22092
    [Google Scholar]
  116. 116.
    Sgritta M, Dooling SW, Buffington SA, Momin EN, Francis MB et al. 2019. Mechanisms underlying microbial-mediated changes in social behavior in mouse models of autism spectrum disorder. Neuron 101:2246–59.e6
    [Google Scholar]
  117. 117.
    Shulkin M, Pimpin L, Bellinger D, Kranz S, Fawzi W et al. 2018. n-3 fatty acid supplementation in mothers, preterm infants, and term infants and childhood psychomotor and visual development: a systematic review and meta-analysis. J. Nutr. 148:3409–18
    [Google Scholar]
  118. 118.
    Simpson JB, Redinbo MR. 2022. Multi-omic analysis of host–microbial interactions central to the gut–brain axis. Mol. Omics 18:10896–907
    [Google Scholar]
  119. 119.
    Singh H. 2006. The milk fat globule membrane—a biophysical system for food applications. Curr. Opin. Colloid Interface Sci. 11:2/3154–63
    [Google Scholar]
  120. 120.
    Slykerman RF, Coomarasamy C, Wickens K, Thompson JMD, Stanley TV et al. 2019. Exposure to antibiotics in the first 24 months of life and neurocognitive outcomes at 11 years of age. Psychopharmacology 236:51573–82
    [Google Scholar]
  121. 121.
    Slykerman RF, Kang J, Van Zyl N, Barthow C, Wickens K et al. 2018. Effect of early probiotic supplementation on childhood cognition, behaviour and mood a randomised, placebo-controlled trial. Acta Paediatr. 107:122172–78
    [Google Scholar]
  122. 122.
    Spitsberg VL. 2005. Bovine milk fat globule membrane as a potential nutraceutical. J. Dairy Sci. 88:72289–94
    [Google Scholar]
  123. 123.
    Stirling F, Naydich A, Bramante J, Barocio R, Certo M et al. 2020. Synthetic cassettes for pH-mediated sensing, counting, and containment. Cell Rep. 30:93139–48.e4
    [Google Scholar]
  124. 124.
    Strati F, Cavalieri D, Albanese D, De Felice C, Donati C et al. 2017. New evidences on the altered gut microbiota in autism spectrum disorders. Microbiome 5:24
    [Google Scholar]
  125. 125.
    Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N et al. 2004. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J. Physiol. 558:1263–75
    [Google Scholar]
  126. 126.
    Sugino KY, Hernandez TL, Barbour LA, Kofonow JM, Frank DN, Friedman JE. 2022. A maternal higher-complex carbohydrate diet increases bifidobacteria and alters early life acquisition of the infant microbiome in women with gestational diabetes mellitus. Front. Endocrinol. 13:921464
    [Google Scholar]
  127. 127.
    Surzenko N, Pjetri E, Munson CA, Friday WB, Hauser J, Mitchell ES. 2020. Prenatal exposure to the probiotic Lactococcus lactis decreases anxiety-like behavior and modulates cortical cytoarchitecture in a sex specific manner. PLOS ONE 15:7e0223395
    [Google Scholar]
  128. 128.
    Szklany K, Engen PA, Naqib A, Green SJ, Keshavarzian A et al. 2022. Dietary supplementation throughout life with non-digestible oligosaccharides and/or n-3 poly-unsaturated fatty acids in healthy mice modulates the gut–immune system–brain axis. Nutrients 14:1173
    [Google Scholar]
  129. 129.
    Tarr AJ, Galley JD, Fisher SE, Chichlowski M, Berg BM, Bailey MT. 2015. The prebiotics 3′sialyllactose and 6′sialyllactose diminish stressor-induced anxiety-like behavior and colonic microbiota alterations: evidence for effects on the gut-brain axis. Brain Behav. Immun. 50:166–77
    [Google Scholar]
  130. 130.
    Thänert R, Sawhney SS, Schwartz DJ, Dantas G. 2022. The resistance within: antibiotic disruption of the gut microbiome and resistome dynamics in infancy. Cell Host Microbe 30:5675–83
    [Google Scholar]
  131. 131.
    Timby N, Domellöf E, Hernell O, Lönnerdal B, Domellöf M. 2014. Neurodevelopment, nutrition, and growth until 12 mo of age in infants fed a low-energy, low-protein formula supplemented with bovine milk fat globule membranes: a randomized controlled trial. Am. J. Clin. Nutr. 99:4860–68
    [Google Scholar]
  132. 132.
    Urbonaite G, Knyzeliene A, Bunn FS, Smalskys A, Neniskyte U. 2022. The impact of maternal high-fat diet on offspring neurodevelopment. Front. Neurosci. 16:909762
    [Google Scholar]
  133. 133.
    Valentine CJ, Wagner CL. 2013. Nutritional management of the breastfeeding dyad. Pediatr. Clin. N. Am. 60:1261–74
    [Google Scholar]
  134. 134.
    van Mil NH, Steegers-Theunissen RPM, Motazedi E, Jansen PW, Jaddoe VWV et al. 2015. Low and high birth weight and the risk of child attention problems. J. Pediatr. 166:4862–63
    [Google Scholar]
  135. 135.
    Vandenplas Y, Analitis A, Tziouvara C, Kountzoglou A, Drakou A et al. 2017. Safety of a new synbiotic starter formula. Pediatr. Gastroenterol. Hepatol. Nutr. 20:3167–77
    [Google Scholar]
  136. 136.
    Vandenplas Y, de Halleux V, Arciszewska M, Lach P, Pokhylko V et al. 2020. A partly fermented infant formula with postbiotics including 3′-GL, specific oligosaccharides, 2′-FL, and milk fat supports adequate growth, is safe and well-tolerated in healthy term infants: a double-blind, randomised, controlled, multi-country trial. Nutrients 12:113560
    [Google Scholar]
  137. 137.
    Victora CG, Bahl R, Barros AJD, França GVA, Horton S et al. 2016. Breastfeeding in the 21st century: epidemiology, mechanisms, and lifelong effect. Lancet 387:10017475–90
    [Google Scholar]
  138. 138.
    Volker E, Tessier C, Rodriguez N, Yager J, Kozyrskyj A. 2022. Pathways of atopic disease and neurodevelopmental impairment: assessing the evidence for infant antibiotics. Expert Rev. Clin. Immunol. 18:9901–22
    [Google Scholar]
  139. 139.
    Vuong H. 2022. Intersections of the microbiome and early neurodevelopment. Int. Rev. Neurobiol. 167:1–23
    [Google Scholar]
  140. 140.
    Vuong HE, Pronovost GN, Williams DW, Coley EJL, Siegler EL et al. 2020. The maternal microbiome modulates fetal neurodevelopment in mice. Nature 586:7828281–86
    [Google Scholar]
  141. 141.
    Wang Y, Li N, Yang J-J, Zhao D-M, Chen B et al. 2020. Probiotics and fructo-oligosaccharide intervention modulate the microbiota–gut–brain axis to improve autism spectrum reducing also the hyper-serotonergic state and the dopamine metabolism disorder. Pharmacol. Res. 157:104784
    [Google Scholar]
  142. 142.
    Willing BP, Russell SL, Finlay BB. 2011. Shifting the balance: antibiotic effects on host-microbiota mutualism. Nat. Rev. Microbiol. 9:4233–43
    [Google Scholar]
  143. 143.
    Windham GC, Anderson M, Lyall K, Daniels JL, Kral TVE et al. 2019. Maternal pre-pregnancy body mass index and gestational weight gain in relation to autism spectrum disorder and other developmental disorders in offspring. Autism Res. 12:2316–27
    [Google Scholar]
  144. 144.
    Wu Y, Wang Y, Hu A, Shu X, Huang W et al. 2022. Lactobacillus plantarum–derived postbiotics prevent Salmonella-induced neurological dysfunctions by modulating gut–brain axis in mice. Front. Nutr. 9:946096
    [Google Scholar]
  145. 145.
    Xu T, Wu X, Liu J, Sun J, Wang X et al. 2022. The regulatory roles of dietary fibers on host health via gut microbiota–derived short chain fatty acids. Curr. Opin. Pharmacol. 62:36–42
    [Google Scholar]
  146. 146.
    Yano JM, Yu K, Donaldson GP, Shastri GG, Ann P et al. 2015. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161:2264–76
    [Google Scholar]
  147. 147.
    Yuan Q, Gong H, Du M, Li T, Mao X. 2022. Milk fat globule membrane supplementation to obese rats during pregnancy and lactation promotes neurodevelopment in offspring via modulating gut microbiota. Front. Nutr. 9:945052
    [Google Scholar]
  148. 148.
    Zhang T, Sidorchuk A, Sevilla-Cermeño L, Vilaplana-Pérez A, Chang Z et al. 2019. Association of cesarean delivery with risk of neurodevelopmental and psychiatric disorders in the offspring: a systematic review and meta-analysis. JAMA Netw. Open 2:8e1910236
    [Google Scholar]
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