A Review on Maternal and Infant Microbiota and Their Implications for the Prevention and Treatment of Allergic Diseases

Allergic diseases, which are closely related to the composition and metabolism of maternal and infant flora, are prevalent in infants worldwide. The mother’s breast milk, intestinal, and vaginal flora directly or indirectly influence the development of the infant’s immune system from pregnancy to lactation, and the compositional and functional alterations of maternal flora are associated with allergic diseases in infants. Meanwhile, the infant’s own flora, represented by the intestinal flora, indicates and regulates the occurrence of allergic diseases and is altered with the intervention of allergic diseases. By searching and selecting relevant literature in PubMed from 2010 to 2023, the mechanisms of allergy development in infants and the links between maternal and infant flora and infant allergic diseases are reviewed, including the effects of flora composition and its consequences on infant metabolism. The critical role of maternal and infant flora in allergic diseases has provided a window for probiotics as a microbial therapy. Therefore, the uses and mechanisms by which probiotics, such as lactic acid bacteria, can help to improve the homeostasis of both the mother and the infant, and thereby treat allergies, are also described.

[1]  Wen-Wei Chang,et al.  Lacticaseibacillus paracasei GM-080 Ameliorates Allergic Airway Inflammation in Children with Allergic Rhinitis: From an Animal Model to a Double-Blind, Randomized, Placebo-Controlled Trial , 2023, Cells.

[2]  Bu-Zhen Tan,et al.  Commercial probiotic products in public health: current status and potential limitations , 2023, Critical reviews in food science and nutrition.

[3]  Y. Sung,et al.  Combined IgE neutralization and Bifidobacterium longum supplementation reduces the allergic response in models of food allergy , 2022, Nature Communications.

[4]  Kathrine L. Barnes,et al.  Heritable vaginal bacteria influence immune tolerance and relate to early-life markers of allergic sensitization in infancy , 2022, Cell reports. Medicine.

[5]  Steven Smriga,et al.  Dosing a synbiotic of human milk oligosaccharides and B. infantis leads to reversible engraftment in healthy adult microbiomes without antibiotics. , 2022, Cell host & microbe.

[6]  Hao Zhang,et al.  Bifidobacterium longum mediated tryptophan metabolism to improve atopic dermatitis via the gut-skin axis , 2022, Gut microbes.

[7]  M. Tang,et al.  Probiotic peanut oral immunotherapy versus oral immunotherapy and placebo in children with peanut allergy in Australia (PPOIT-003): a multicentre, randomised, phase 2b trial. , 2022, The Lancet. Child & adolescent health.

[8]  F. Carmona,et al.  Efficacy of Probiotics in Children and Adolescents With Atopic Dermatitis: A Randomized, Double-Blind, Placebo-Controlled Study , 2022, Frontiers in Nutrition.

[9]  L. Drago,et al.  The Probiotics in Pediatric Asthma Management (PROPAM) Study in the Primary Care Setting: A Randomized, Controlled, Double-Blind Trial with Ligilactobacillus salivarius LS01 (DSM 22775) and Bifidobacterium breve B632 (DSM 24706) , 2022, Journal of immunology research.

[10]  Yuan Wei,et al.  Association Between Breastmilk Microbiota and Food Allergy in Infants , 2022, Frontiers in Cellular and Infection Microbiology.

[11]  Thomas P. Quinn,et al.  The maternal gut microbiome during pregnancy and offspring allergy and asthma. , 2021, The Journal of allergy and clinical immunology.

[12]  C. Akdis Does the epithelial barrier hypothesis explain the increase in allergy, autoimmunity and other chronic conditions? , 2021, Nature Reviews Immunology.

[13]  Lanwei Zhang,et al.  Breast milk flora plays an important role in infantile eczema: cohort study in Northeast China , 2021, Journal of applied microbiology.

[14]  F. Olivero,et al.  Treatment with a Probiotic Mixture Containing Bifidobacterium animalis Subsp. Lactis BB12 and Enterococcus faecium L3 for the Prevention of Allergic Rhinitis Symptoms in Children: A Randomized Controlled Trial , 2021, Nutrients.

[15]  T. Chatila,et al.  The Microbial Origins of Food Allergy. , 2020, The Journal of allergy and clinical immunology.

[16]  You-jin Jang,et al.  Lactobacillus paracasei KBL382 administration attenuates atopic dermatitis by modulating immune response and gut microbiota , 2020, Gut microbes.

[17]  Jinrong Fu,et al.  Research Progress in Atopic March , 2020, Frontiers in Immunology.

[18]  Hye‐Ryun Kang,et al.  Probiotic NVP-1703 Alleviates Allergic Rhinitis by Inducing IL-10 Expression: A Four-week Clinical Trial , 2020, Nutrients.

[19]  J. Carlin,et al.  Maternal carriage of Prevotella during pregnancy associates with protection against food allergy in the offspring , 2020, Nature Communications.

[20]  M. Sears,et al.  Reduced genetic potential for butyrate fermentation in the gut microbiome of infants who develop allergic sensitization. , 2019, The Journal of allergy and clinical immunology.

[21]  T. Bale,et al.  Prenatal and postnatal contributions of the maternal microbiome on offspring programming , 2019, Frontiers in Neuroendocrinology.

[22]  E. Segal,et al.  The pros, cons, and many unknowns of probiotics , 2019, Nature Medicine.

[23]  C. Mølgaard,et al.  Probiotics in late infancy reduce the incidence of eczema: A randomized controlled trial , 2019, Pediatric allergy and immunology : official publication of the European Society of Pediatric Allergy and Immunology.

[24]  J. Garssen,et al.  Gut microbiota from infant with cow’s milk allergy promotes clinical and immune features of atopy in a murine model , 2019, Allergy.

[25]  Ting Zhang,et al.  Akkermansia muciniphila is a promising probiotic , 2019, Microbial biotechnology.

[26]  E. Savilahti,et al.  Perinatal probiotic intervention prevented allergic disease in a Caesarean‐delivered subgroup at 13‐year follow‐up , 2019, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[27]  J. Gisbert,et al.  Microbiota Sensing by Mincle-Syk Axis in Dendritic Cells Regulates Interleukin-17 and -22 Production and Promotes Intestinal Barrier Integrity , 2019, Immunity.

[28]  B. Finlay,et al.  Association between the intestinal microbiota and allergic sensitization, eczema, and asthma: A systematic review , 2019, The Journal of allergy and clinical immunology.

[29]  R. Knight,et al.  Role of the microbiome in human development , 2019, Gut.

[30]  A. Yılmaz,et al.  Investigation of the Efficacy of Lactobacillus rhamnosus GG in Infants With Cow’s Milk Protein Allergy: a Randomised Double-Blind Placebo-Controlled Trial , 2019, Probiotics and Antimicrobial Proteins.

[31]  D. Antonopoulos,et al.  Healthy infants harbor intestinal bacteria that protect against food allergy , 2018, Nature Medicine.

[32]  E. Mitchell,et al.  Effects of Lactobacillus rhamnosus HN001 in early life on the cumulative prevalence of allergic disease to 11 years , 2018, Pediatric allergy and immunology : official publication of the European Society of Pediatric Allergy and Immunology.

[33]  C. S. C. Tan-Lim,et al.  Probiotics as treatment for food allergies among pediatric patients: a meta-analysis , 2018, The World Allergy Organization journal.

[34]  L. Engstrand,et al.  Temporal and long‐term gut microbiota variation in allergic disease: A prospective study from infancy to school age , 2018, Allergy.

[35]  S. Seys,et al.  Intranasal administration of probiotic Lactobacillus rhamnosus GG prevents birch pollen‐induced allergic asthma in a murine model , 2018, Allergy.

[36]  M. Jenmalm,et al.  Oral microbiota maturation during the first 7 years of life in relation to allergy development , 2018, Allergy.

[37]  Jop de Vrieze The metawars. , 2018, Science.

[38]  H. Szajewska,et al.  Lactobacillus rhamnosus GG in the Primary Prevention of Eczema in Children: A Systematic Review and Meta-Analysis , 2018, Nutrients.

[39]  Namhee Kim,et al.  Lactobacillus sakei WIKIM30 Ameliorates Atopic Dermatitis-Like Skin Lesions by Inducing Regulatory T Cells and Altering Gut Microbiota Structure in Mice , 2018, Front. Immunol..

[40]  A. Mowat To respond or not to respond — a personal perspective of intestinal tolerance , 2018, Nature Reviews Immunology.

[41]  D. Elston,et al.  When worlds collide: Th17 and Treg cells in cancer and autoimmunity , 2018, Cellular & Molecular Immunology.

[42]  G. Wong,et al.  Pediatric allergy and immunology in China , 2018, Pediatric allergy and immunology : official publication of the European Society of Pediatric Allergy and Immunology.

[43]  P. Pannaraj,et al.  Mother’s Milk: A Purposeful Contribution to the Development of the Infant Microbiota and Immunity , 2018, Front. Immunol..

[44]  M. Cabana,et al.  Delayed gut microbiota development in high-risk for asthma infants is temporarily modifiable by Lactobacillus supplementation , 2018, Nature Communications.

[45]  S. Nordlander,et al.  Early-Life Human Microbiota Associated With Childhood Allergy Promotes the T Helper 17 Axis in Mice , 2017, Front. Immunol..

[46]  L. Drago,et al.  Role of the Human Breast Milk-Associated Microbiota on the Newborns’ Immune System: A Mini Review , 2017, Front. Microbiol..

[47]  So‐ichiro Hirata,et al.  Gut microbiome, metabolome, and allergic diseases. , 2017, Allergology international : official journal of the Japanese Society of Allergology.

[48]  Ruixue Huang,et al.  Probiotics for the Treatment of Atopic Dermatitis in Children: A Systematic Review and Meta-Analysis of Randomized Controlled Trials , 2017, Front. Cell. Infect. Microbiol..

[49]  M. Cabana,et al.  Early Probiotic Supplementation for Eczema and Asthma Prevention: A Randomized Controlled Trial , 2017, Pediatrics.

[50]  Harsh Panwar,et al.  Bacillus As Potential Probiotics: Status, Concerns, and Future Perspectives , 2017, Front. Microbiol..

[51]  Y. Yamashiro,et al.  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 , 2017, Front. Microbiol..

[52]  Kyle Bittinger,et al.  Association Between Breast Milk Bacterial Communities and Establishment and Development of the Infant Gut Microbiome , 2017, JAMA pediatrics.

[53]  A. K. Hansen,et al.  Sensitivity to oxazolone induced dermatitis is transferable with gut microbiota in mice , 2017, Scientific Reports.

[54]  M. Jenmalm,et al.  Aberrant IgA responses to the gut microbiota during infancy precede asthma and allergy development , 2017, The Journal of allergy and clinical immunology.

[55]  H. Kong,et al.  Skin microbiome before development of atopic dermatitis: Early colonization with commensal staphylococci at 2 months is associated with a lower risk of atopic dermatitis at 1 year , 2017, The Journal of allergy and clinical immunology.

[56]  S. Salminen,et al.  The human milk microbiome and factors influencing its composition and activity. , 2016, Seminars in fetal & neonatal medicine.

[57]  A. Fiocchi,et al.  Probiotics, Prebiotics & Food allergy Prevention: Clinical Data in Children. , 2016, Journal of pediatric gastroenterology and nutrition.

[58]  Eric A. Franzosa,et al.  Variation in Microbiome LPS Immunogenicity Contributes to Autoimmunity in Humans , 2016, Cell.

[59]  A. Mira,et al.  Relationship between Milk Microbiota, Bacterial Load, Macronutrients, and Human Cells during Lactation , 2016, Front. Microbiol..

[60]  Shumei S. Sun,et al.  A Randomized Controlled Trial Assessing Growth of Infants Fed a 100% Whey Extensively Hydrolyzed Formula Compared With a Casein-Based Extensively Hydrolyzed Formula , 2016, Global pediatric health.

[61]  G. Gloor,et al.  Human milk microbiota profiles in relation to birthing method, gestation and infant gender , 2016, Microbiome.

[62]  N. Kapel,et al.  Three Novel Candidate Probiotic Strains with Prophylactic Properties in a Murine Model of Cow's Milk Allergy , 2016, Applied and Environmental Microbiology.

[63]  A. Mira,et al.  Impact of mode of delivery on the milk microbiota composition of healthy women , 2015, Journal of Developmental Origins of Health and Disease.

[64]  M. Inouye,et al.  The Infant Nasopharyngeal Microbiome Impacts Severity of Lower Respiratory Infection and Risk of Asthma Development , 2015, Cell Host & Microbe.

[65]  J. M. Rodríguez The origin of human milk bacteria: is there a bacterial entero-mammary pathway during late pregnancy and lactation? , 2014, Advances in nutrition.

[66]  K. McCoy,et al.  Intestinal Microbial Diversity during Early-Life Colonization Shapes Long-Term IgE Levels , 2013, Cell host & microbe.

[67]  I. Ioshikhes,et al.  Human milk metagenome: a functional capacity analysis , 2013, BMC Microbiology.

[68]  Christian Milani,et al.  Bacteria as vitamin suppliers to their host: a gut microbiota perspective. , 2013, Current opinion in biotechnology.

[69]  W. Walker,et al.  The role of gut microbiota in programming the immune phenotype , 2013, Journal of Developmental Origins of Health and Disease.

[70]  S. Salminen,et al.  The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. , 2012, The American journal of clinical nutrition.

[71]  Jonathan Friedman,et al.  Inferring Correlation Networks from Genomic Survey Data , 2012, PLoS Comput. Biol..

[72]  J. Celedón,et al.  Maternal intestinal flora and wheeze in early childhood , 2012, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[73]  R. Berni Canani,et al.  The Potential Therapeutic Efficacy of Lactobacillus GG in Children with Food Allergies , 2012, Pharmaceuticals.

[74]  H. McShane,et al.  Th1/Th17 Cell Induction and Corresponding Reduction in ATP Consumption following Vaccination with the Novel Mycobacterium tuberculosis Vaccine MVA85A , 2011, PloS one.

[75]  Ursel M. E. Schütte,et al.  Characterization of the Diversity and Temporal Stability of Bacterial Communities in Human Milk , 2011, PloS one.

[76]  F. Pérez-Cano,et al.  In vitro immunomodulatory activity of Lactobacillus fermentum CECT5716 and Lactobacillus salivarius CECT5713: two probiotic strains isolated from human breast milk. , 2010, Immunobiology.

[77]  J. M. Rodríguez,et al.  Treatment of infectious mastitis during lactation: antibiotics versus oral administration of Lactobacilli isolated from breast milk. , 2010, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[78]  W. Paul,et al.  Differentiation of effector CD4 T cell populations (*). , 2010, Annual review of immunology.

[79]  C. Edwards,et al.  Changes in faecal microbiota of infants with cow’s milk protein allergy – a Spanish prospective case–control 6‐month follow‐up study , 2010, Pediatric allergy and immunology : official publication of the European Society of Pediatric Allergy and Immunology.

[80]  N. Laforgia,et al.  Lactobacillus GG improves recovery in infants with blood in the stools and presumptive allergic colitis compared with extensively hydrolyzed formula alone. , 2010, The Journal of pediatrics.

[81]  G. Valdez,et al.  Hydrolysis of whey proteins by Lactobacillus acidophilus, Streptococcus thermophilus and Lactobacillus delbrueckii ssp. bulgaricus grown in a chemically defined medium , 2007, Journal of applied microbiology.

[82]  Hans Bisgaard,et al.  Childhood asthma after bacterial colonization of the airway in neonates. , 2007, The New England journal of medicine.

[83]  W. Chey,et al.  The Utility of Probiotics in the Treatment of Irritable Bowel Syndrome: A Systematic Review , 2007, The American Journal of Gastroenterology.

[84]  L. N. Fink,et al.  Epithelial cells prime the immune response to an array of gut‐derived commensals towards a tolerogenic phenotype through distinct actions of thymic stromal lymphopoietin and transforming growth factor‐β , 2007, Immunology.

[85]  J. Xaus,et al.  Two Lactobacillus strains, isolated from breast milk, differently modulate the immune response , 2007, Journal of applied microbiology.

[86]  J. Casanova,et al.  Inborn errors of IL-12/23- and IFN-γ-mediated immunity: molecular, cellular, and clinical features , 2006 .

[87]  L. Fouser,et al.  Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides , 2006, The Journal of experimental medicine.

[88]  J. Xaus,et al.  Antimicrobial potential of four Lactobacillus strains isolated from breast milk , 2006, Journal of applied microbiology.

[89]  C. Akdis,et al.  Induction of interleukin‐10 and suppressor of cytokine signalling‐3 gene expression following peptide immunotherapy , 2006, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[90]  S. Mazmanian,et al.  An Immunomodulatory Molecule of Symbiotic Bacteria Directs Maturation of the Host Immune System , 2005, Cell.

[91]  G. Ruthel,et al.  Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[92]  K. Michaelsen,et al.  Effect of probiotics on gastrointestinal symptoms and small intestinal permeability in children with atopic dermatitis. , 2004, The Journal of pediatrics.

[93]  R. Korpela,et al.  Lactobacillus GG effect in increasing IFN-gamma production in infants with cow's milk allergy. , 2004, The Journal of allergy and clinical immunology.

[94]  A. Macpherson,et al.  Interactions between commensal intestinal bacteria and the immune system , 2004, Nature Reviews Immunology.

[95]  P. Hartmann,et al.  Ultrasound imaging of milk ejection in the breast of lactating women. , 2004, Pediatrics.

[96]  A. Sabrá,et al.  IgE and non-IgE food allergy. , 2003, Annals of allergy, asthma & immunology : official publication of the American College of Allergy, Asthma, & Immunology.

[97]  Marek Jutel,et al.  IL‐10 and TGF‐β cooperate in the regulatory T cell response to mucosal allergens in normal immunity and specific immunotherapy , 2003, European journal of immunology.

[98]  A. Stadnyk Intestinal epithelial cells as a source of inflammatory cytokines and chemokines. , 2002, Canadian journal of gastroenterology = Journal canadien de gastroenterologie.

[99]  P. Holt,et al.  Cellular immune responses to ovalbumin and house dust mite in egg‐allergic children , 2002, Allergy.

[100]  Q. Hamid,et al.  IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. , 2001, The Journal of allergy and clinical immunology.

[101]  D. Corda,et al.  CD28 co‐stimulates TCR/CD3‐induced phosphoinositide turnover in human T lymphocytes , 2001, European journal of immunology.

[102]  T. Kaisho,et al.  Dendritic-cell function in Toll-like receptor- and MyD88-knockout mice. , 2001, Trends in immunology.

[103]  Y. Benno,et al.  Comparison of mucosal adhesion and species identification of bifidobacteria isolated from healthy and allergic infants. , 2001, FEMS immunology and medical microbiology.

[104]  R. Modlin Immunology: A Toll for DNA vaccines , 2000, Nature.

[105]  C. Yeatman,et al.  Inhibition of Kit expression by IL-4 and IL-10 in murine mast cells: role of STAT6 and phosphatidylinositol 3'-kinase. , 1999, Journal of immunology.

[106]  L. Jedrychowski Reduction of the antigenicity of whey proteins by lactic acid fermentation , 1999 .

[107]  P. Naaber,et al.  The intestinal microflora in allergic Estonian and Swedish 2‐year‐old children , 1999, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[108]  C. Mackay,et al.  Chemokines and chemokine receptors in T-cell priming and Th1/Th2-mediated responses. , 1998, Immunology today.

[109]  Richard A Flavell,et al.  The Transcription Factor GATA-3 Is Necessary and Sufficient for Th2 Cytokine Gene Expression in CD4 T Cells , 1997, Cell.

[110]  R. Coffman,et al.  Multiple Pathways for the Initiation of T Helper 2 (Th2) Responses , 1997, The Journal of experimental medicine.

[111]  A. Coyle,et al.  TH2 and 'TH2-like' cells in allergy and asthma: pharmacological perspectives. , 1994, Trends in pharmacological sciences.

[112]  T. Dougherty,et al.  THE USE OF STEROIDS AS ANTI‐INFLAMMATORY AGENTS , 1955, Annals of the New York Academy of Sciences.

[113]  D. Sinderen,et al.  Bifidobacteria and the infant gut: an example of co-evolution and natural selection , 2017, Cellular and Molecular Life Sciences.

[114]  M. Longnecker,et al.  Probiotic milk consumption in pregnancy and infancy and subsequent childhood allergic diseases. , 2014, The Journal of allergy and clinical immunology.

[115]  J. Casanova,et al.  Inborn errors of IL-12/23- and IFN-gamma-mediated immunity: molecular, cellular, and clinical features. , 2006, Seminars in immunology.

[116]  Steve L Taylor,et al.  Factors affecting the determination of threshold doses for allergenic foods: how much is too much? , 2002, The Journal of allergy and clinical immunology.

[117]  N. Osna,et al.  Regulation of interleukin-10 secretion by histamine in TH2 cells and splenocytes. , 2001, International immunopharmacology.