Initial Intestinal Colonization in the Human Infant and Immune Homeostasis
Abstract
The paradigm of disease burden in the developed world has changed drastically in the last few decades from predominately infections to immune-mediated diseases (autoimmunity and allergy) because of alterations in the Western lifestyle (improved sanitation, immunizations, antibiotic usage and altered dietary intake). A diverse balanced microbiota is necessary for the development of an appropriate innate and adaptive immune response. There is strong evidence that disruption of the normal colonization process can lead to alterations in the important symbiotic relationship that is necessary for immune homeostasis. For example, infants born by cesarean section or receiving excessive perinatal antibiotics have inadequate initial colonization and aberrant mucosal immune function. As a result, later in childhood, they express an increased incidence in asthma and autoimmune diseases (e.g. celiac disease). An important component of initial colonization is the infant's diet. Breast milk contains a variety of nondigestible oligosaccharides which function as prebiotics preferentially stimulating proliferation of Bifidobacteria and Lactobacilli, important health-promoting bacteria, and cause fermentation of the oligosaccharides into short-chain fatty acids. In the absence of breastfeeding for the first 6 months of life, formula containing pre- and probiotics may overcome an initial inadequate colonization process and help establish a normal mucosal immune system.
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High consumption of oligosaccharides favors growth of Bifidobacteria, which is the dominant genus of breast-fed infants, who receive most of their carbohydrate as breast milk oligosaccharides.
“High consumption of oligosaccharides favors growth of Bifidobacteria, which is the dominant genus of breast-fed infants, who receive most of their carbohydrate in the form of breast milk oligosaccharides.149”
From The Gut Microbiome and the Brain (2014) · cites this paper as [149]
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Skin-to-Skin Care and the Development of the Preterm Infant Oral Microbiome
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“In humans, the Lactobacilli are particularly present in the gastrointestinal tract and vagina (Walter, 2008) and, along with the Bifidobacteria, are the first bacteria which are colonized in the gut at postnatal age (Walker, 2013).”
BackgroundInfant Complementary Feeding of Prebiotics for the Microbiome and Immunity
McKeen, S., Young, W., Mullaney, J. A., Fraser, K., McNabb, W. C., & Roy, N. C. (2019) · Nutrients · doi:10.3390/nu11020364 · Cited by 65 · see citing works
Microbiome to Brain: Unravelling the Multidirectional Axes of Communication
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“Early colonization is also linked to activation of the hypothalamic-pituitary-adrenal (HPA) axis, which in turn impacts the enteric nervous system (ENS) that innervates the GI tract (Borre et al. 2014 ; Walker 2013 ).”
BackgroundThe Eukaryotic Microbiome: Origins and Implications for Fetal and Neonatal Life
Miller, W. B. (2016) · Frontiers in Pediatrics · doi:10.3389/fped.2016.00096 · Cited by 65 · see citing works
“org September 2016 | Volume 4 | Article 96 to microbial colonization with a resultant breach of the intestinal epithelial barrier involving a breakdown of intestinal immune homeostasis (86, 87).”
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“This early microbiota is expected to be particularly sensitive to a potential modulation by probiotic administration, especially in infants born by cesarean (C)-section (2).”
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“Components of bacteria can trigger toll-like receptors (TLRs), which propagate both innate and adaptive immune responses (186) in resident leukocytes and epithelial cells.”
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“HMO enhance growth [1] [2] and adhesion [3] of probiotic bacteria to gut epithelial cells.”
The Use of Fecal Microbiome Transplant in Treating Human Diseases: Too Early for Poop?
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“Moreover, antibiotics use during intrapartum have been shown to be associated with overall microbial composition in breast milk including decreased levels of protective bacteria like Bifidobacteria, which then led to the concern that infant would benefit less from drinking the mother’s breast milk and place them at a…”
BackgroundMetabolic Interaction of Helicobacter pylori Infection and Gut Microbiota
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“Gut microbial communities are known to be inherited from the mother [2,3].”
BackgroundAntimicrobial Prophylaxis for Children with Vesicoureteral Reflux
Hoberman, A., & Chesney, R. W. (2014) · New England Journal of Medicine · doi:10.1056/nejmc1408559 · Cited by 50 · see citing works
Applying Precision Public Health to Prevent Preterm Birth
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Development of the infant intestinal microbiome: A bird's eye view of a complex process
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“The more recent term: the “microflora hypothesis” acknowledges a mediating role for dysbiotic distortion of immunologic tolerance caused by antibiotics and/or other modern environmental influences (Noverr and Huffnagle, 2005; Walker, 2013).”
B Regulatory Cells: Players in Pregnancy and Early Life
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Noninvasive molecular fingerprinting of host–microbiome interactions in neonates
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“Recently, Walker [37] proposed that a diverse balanced microbiota is necessary for the development of an appropriate innate and adaptive immune response.”
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“There is considerable interest in the connection between the composition of the infant gut microbiota and late-life risk for asthma, allergy and autoimmune-type diseases (reviewed in((26))), particularly because of the soaring rate of births by caesarean section in many countries((27)).”
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Maternal depressive symptoms linked to reduced fecal Immunoglobulin A concentrations in infants
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“the first few weeks of life until the infant gut begins to produce endogenous sIgA (Battersby and Gibbons, 2013; Walker, 2013).”
BackgroundProbiotics can really cure an autoimmune disease?
Yousefi, B., Eslami, M., Ghasemian, A., Kokhaei, P., & Sadeghnejhad, A. (2019) · Gene Reports · doi:10.1016/j.genrep.2019.100364 · Cited by 43 · see citing works
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“Bifidobacterium has been associated with beneficial effects on immune and intestinal function [17, 18].”
BackgroundCOVID-19: Relationship and Impact on Breastfeeding—A Systematic Review
Pérez-Bermejo, M., Peris-Ochando, B., & Murillo-Llorente, M. T. (2021) · Nutrients · doi:10.3390/nu13092972 · Cited by 42 · see citing works
“In addition, they also play a vital role in the development of a diverse and balanced microbiota, essential for appropriate innate and adaptive immune responses, and help colonise up to 90% of the infant biome [48,51].”
BackgroundFernando, W. M. A. D. B., Flint, S., Ranaweera, K. K. D. S., Bamunuarachchi, A., Johnson, S. K., & Brennan, C. S. (2017) · International Journal of Food Sciences and Nutrition · doi:10.1080/09637486.2017.1340932 · Cited by 41 · see citing works
The microbiota as a component of the celiac disease and non-celiac gluten sensitivity
Nylund, L., Kaukinen, K., & Lindfors, K. (2016) · Clinical Nutrition Experimental · doi:10.1016/j.yclnex.2016.01.002 · Cited by 40 · see citing works
“and Faecalibacterium prausnitzii or Ruminococcus bromii and Eubacterium rectale, respectively [8].”
BackgroundRheumatoid arthritis and the intestinal microbiome: probiotics as a potential therapy
Yang, Y., Hong, Q., Zhang, X., & Liu, Z. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1331486 · Cited by 40 · see citing works
“TLRs are recognized by both gram-positive and gram-negative bacteria to regulate innate and adaptive immunity (48).”
BackgroundEconomic Evaluation of Adjunctive Azithromycin Prophylaxis for Cesarean Delivery
Harper, L. M., Kilgore, M. L., Szychowski, J. M., Andrews, W. W., & Tita, A. (2017) · Obstetrics and Gynecology · doi:10.1097/aog.0000000000002129 · Cited by 39 · see citing works
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Vaccines Against Escherichia coli
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Żeber‐Lubecka, N., Kulecka, M., Ambrożkiewicz, F., Paziewska, A., Lechowicz, M., Konopka, E., Majewska, U., Borszewska-Kornacka, M. K., Mikuła, M., Cukrowská, B., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150306 · Cited by 34 · see citing works
“The normal colonization process is most likely to occur in full-term, vaginally delivered, and breastfed infants [1], while misdirected development of the gut bacterial community in preterm infants may affect the gut and immune function, leading to severe diseases such as necrotizing enterocolitis (NEC) [8–10].”
BackgroundAmoxicillin-Clavulanic Acid Resistance in the Genus Bifidobacterium
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Intestinal Microbiota in Common Chronic Inflammatory Disorders Affecting Children
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“Perturbations in the Human Gut Microbiota There are several factors that can influence intestinal homeostasis, including cesarean delivery, feeding infant formula instead of breastfeeding, antibiotics, diet, geography, and hygiene (66) (Figure 2).”
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The role of the gut microbiome in mediating neurotoxic outcomes to PCB exposure
Rude, K. M., Keogh, C. E., & Gareau, M. G. (2019) · NeuroToxicology · doi:10.1016/j.neuro.2019.08.010 · Cited by 31 · see citing works
“Furthermore, perturbations in the gut microbiome in early life increases susceptibility to a number of immune-related pathologies such as inflammatory bowel disease (IBD) and asthma (Walker, 2013).”
BackgroundMaternal psychological distress before birth influences gut immunity in mid‐infancy
Kang, L. J., Vu, K. N., Koleva, P. T., Field, C. J., Chow, A., Azad, M. B., Becker, A. B., Mandhane, P. J., Moraes, T. J., Sears, M. R., et al. (2019) · Clinical & Experimental Allergy · doi:10.1111/cea.13551 · Cited by 28 · see citing works
Gut microbiota biomodulators, when the stork comes by the scalpel
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“Clinical evidence suggests that probiotics can act as surrogate colonizers [13] and help prevent the expression of allergic diseases.”
BackgroundCystic fibrosis: An update for clinicians. Part 1: Nutrition and gastrointestinal complications
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Impact of Prebiotics on Enteric Diseases and Oxidative Stress
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“Intestinal microbiota and its metabolites play a major role in defining the antigen milieu of enterocytes, since they are able to interfere with the cells of the intestinal epithelium and modulate the signaling pathways through specific receptors [10].”
BackgroundTET2 and TET3 loss disrupts small intestine differentiation and homeostasis
Ansari, I., Solé‐Boldo, L., Ridnik, M., Gutekunst, J., Gilliam, O., Korshko, M., Liwinski, T., Jickeli, B., Weinberg-Corem, N., Shoshkes-Carmel, M., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-39512-3 · Cited by 23 · see citing works
DNA methylation as a regulator of intestinal gene expression
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Human Milk Bactericidal Properties
Salcedo, J., Gormáz, M., López‐Mendoza, M. C., Nogarotto, E., & Silvestre, D. (2014) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000000641 · Cited by 22 · see citing works
“The bactericidal capacity and microbiota of human milk are 2 properties that contribute to a specific intestinal colonization (5).”
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“Un zation with more Bifidobacteria and Lactobacilli, and less potential pathogens (48).”
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“Human milk oligosaccharides (hMOs) as the third most abundant nutrient after lactose and lipids in human milk are considered to be highly significant in this guidance (Allan Walker 2013; Smilowitz et al. 2014; Zuurveld et al. 2020).”
A primer on investigating the role of the microbiome in brain and cognitive development
Kelsey, C. M., Dreisbach, C., Alhusen, J. L., & Großmann, T. (2018) · Developmental Psychobiology · doi:10.1002/dev.21778 · Cited by 20 · see citing works
Bacterial Colonization of the Newborn Gut, Immune Development, and Prevention of Disease
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Self-citationRisk of Celiac Disease According to HLA Haplotype and Country
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Signs and symptoms associated with digestive tract development
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“Cesarean delivery has been associated with a delayed and dysbalanced intestinal colonization in newborns [43–45] and an increased risk of asthma [46] and other immune diseases [47,48].”
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Microbial Physiology of the Digestive Tract and Its Role in Inflammatory Bowel Diseases
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Epigenome-Wide Association of Infant Feeding and Changes in DNA Methylation from Birth to 10 Years
Mallisetty, Y., Mukherjee, N., Jiang, Y., Chen, S., Ewart, S., Arshad, S. H., Holloway, J. W., Zhang, H., & Karmaus, W. (2020) · Nutrients · doi:10.3390/nu13010099 · Cited by 18 · see citing works
Effect of Food Endotoxin on Infant Health
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Montero, C. G., Fraile‐Μartinez, O., Rodriguez-Martín, S., Saz, J. V., Rodríguez, R. A., Moreno, J. M. P., Ruiz-Labarta, J., García‐Honduvilla, N., Álvarez‐Mon, M., Bravo, C., et al. (2023) · Foods · doi:10.3390/foods12061148 · Cited by 16 · see citing works
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Adjuvanted Immunotherapy Approaches for Peanut Allergy
Johnson‐Weaver, B. T., Staats, H. F., Burks, A. W., & Kulis, M. D. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02156 · Cited by 16 · see citing works
“Lactobacillus and Bifidobacterium species are common bacteria used for probiotics (19) and may improve peanut allergy.”
BackgroundOemcke, L. A., Anderson, R. C., Altermann, E., Roy, N. C., & McNabb, W. C. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.759137 · Cited by 15 · see citing works
“The complex molecular structures of these milk oligosaccharides are digested by probiotic bacteria which is key for developing a diverse and balanced microbial community in the infant GIT (110).”
BackgroundSarkar, V. K., De, U. K., Kala, A., Verma, A. K., Chauhan, A., Paul, B. R., Soni, S., Gandhar, J. S., Chaudhuri, P., Patra, M. K., et al. (2022) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-022-09964-y · Cited by 15 · see citing works
“Earlier studies showed the importance of the gut microbiota and immune system and their interaction for development of gastrointestinal tract and health on neonates [7].”
BackgroundPrebiotic Activity of Vaginal Lactobacilli on Bifidobacteria: from Concept to Formulation
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“exclusively breastfed during the first 6 months of life (4, 5).”
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“This feed antigen can cause local inflammation in the intestine and increase the production of pro-inflammatory cytokines, such as TNF-α, interleukin-1, and interleukin-6 [30].”
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“This early microbiome is essential for the long-term health of the newborn, influencing susceptibility to inflammatory, metabolic, and autoimmune diseases in childhood and adulthood [185].”
Burn injury influences the T cell homeostasis in a butyrate-acid sphingomyelinase dependent manner
Rice, T. C., Armocida, S. M., Kuethe, J. W., Midura, E. F., Jain, A., Hildeman, D. A., Healy, D. P., Gulbins, E., & Caldwell, C. C. (2016) · Cellular Immunology · doi:10.1016/j.cellimm.2016.12.004 · Cited by 13 · see citing works
“Additionally, use of antibiotics in the neonatal period can alter the intestinal microbiota and has been associated with increased expression of asthma and autoimmune diseases [47, 48].”
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“However, the composition of the individual bacteria in the present study differ from those found in European neonates (21, 23, 24).”
ResultMicrobiota in health and disease: from pregnancy to childhood
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The Life-Long Role of Nutrition on the Gut Microbiome and Gastrointestinal Disease
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- Authors
- Walker, W. A.
- Affiliations
- Harvard University (US)
- Corresponding author
- Walker, W. Allan
- ORCID
- Walker, W. Allan
- Venue
- Annals of Nutrition and Metabolism
- Publisher
- S. Karger AG
- Published
- 2013
- Volume
- 63
- Issue
- Suppl. 2
- Pages
- 8-15
- ISSN
- 0250-6807 (ISSN-L)
- 1421-9697
- OpenAlex
- W2146037987
- Cited by
- 161
- References
- 52
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 6 · 2023: 11 · 2022: 10 · 2021: 20 · 2020: 7 · 2019: 12 · 2018: 10 · 2017: 17 · 2016: 23 · 2015: 21 · 2014: 16
- FWCI
- 2.26
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annals of Nutrition and Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK040561)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Keywords
- infant gut microbiota, immune homeostasis, cesarean section, asthma, autoimmune disease, celiac disease, human milk oligosaccharides, prebiotics, probiotics, infant formula, Bifidobacterium, lactobacilli, short-chain fatty acids, mucosal immunity, Western lifestyle
- MeSH terms
- Asthma, Autoimmune Diseases, Bifidobacterium, Female, Fermentation, Homeostasis, Humans, Immunity, Infant Nutritional Physiological Phenomena, Infant, Newborn, Intestines, Lactobacillus, Milk, Human, Oligosaccharides, Pregnancy, Probiotics, Infant Formula, Prebiotics, Microbiota
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