The Microbiome in Food Allergy and Eosinophilic Esophagitis

  • Alyson L. Yee
  • Mary M. Buschmann
  • Christina E. Ciaccio
  • Jack A. Gilbert


While it has been proposed that the relatively recent rise in human food allergy is linked to an environmental factor, the fundamental understanding of the underlying etiology remains elusive. Disruption of the human microbiome is one mechanism by which the environment could influence immune and physiological dysregulation and potentiate food allergy. The microbiome is the collection of microbial organisms and their genes that co-associate with our bodies. Life style choices, including diet, levels of activity, and the degree of interaction with the outdoor world, are all associated with distinct changes in the metabolic products synthesized by the resident microbiome. The microbiome and its metabolites play an essential role in physiological stability in the human body. Disruption of this homeostasis can lead to a reduction in the synthesis of short chain fatty acids, which can retard intestinal epithelial cell maturity and alter regulatory T-cell differentiation. Additionally, certain life styles can select for the growth of bacteria that produce proinflammatory compounds, such as hydrogen sulfide or lipopolysaccharide. While the mechanisms remain unclear, the literature suggests that host-microbe interactions are central to allergic processes. In this chapter, we explore how microbiome colonization and development early in life are associated with food allergy onset and examine the potential of microbiome-based therapeutics to successfully treat food allergic disorders.


Microbiome Eosinophilic esophagitis Food allergy Immune response Short-chain fatty acids 


  1. 1.
    Sicherer SH, Allen K, Lack G, Taylor SL, Donovan SM, Oria M. Critical issues in food allergy: a national academies consensus report. Pediatrics. 2017;140:e20170194.PubMedCrossRefGoogle Scholar
  2. 2.
    Jackson KD, Howie LD, Akinbami LJ. Trends in allergic conditions among children: United States, 1997–2011. NCHS Data Brief. 2013;121:1–8.Google Scholar
  3. 3.
    Gupta RS, Warren CM, Smith BM, Blumenstock JA, Jiang J, Davis MM, et al. The public health impact of parent-reported childhood food allergies in the United States. Pediatrics. 2018;142(6):e20181235.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Berni Canani R, Paparo L, Nocerino R, Di Scala C, Della Gatta G, Maddalena Y, et al. Gut microbiome as target for innovative strategies against food allergy. Front Immunol. 2019;10:191. Scholar
  5. 5.
    Leung ASY, Wong GWK, Tang MLK. Food allergy in the developing world. J Allergy Clin Immunol. 2018;141:76–78.e1.PubMedCrossRefGoogle Scholar
  6. 6.
    Savage JH, Lee-Sarwar KA, Sordillo J, Bunyavanich S, Zhou Y, O’Connor G, Set a. A prospective microbiome-wide association study of food sensitization and food allergy in early childhood. Allergy. 2018;73:145–52.PubMedCrossRefGoogle Scholar
  7. 7.
    Strachan DP. Hay fever, hygiene, and household size. BMJ. 1989;299:1259–60.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Scudellari M. News feature: cleaning up the hygiene hypothesis. Proc Natl Acad Sci. 2017;114:1433–6.PubMedCrossRefGoogle Scholar
  9. 9.
    Bloomfield SF, Rook GA, Scott EA, Shanahan F, Stanwell-Smith R, Turner P. Time to abandon the hygiene hypothesis: new perspectives on allergic disease, the human microbiome, infectious disease prevention and the role of targeted hygiene. Perspect Public Health. 2016;136:213–24.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Plunkett CH, Nagler CR. 2017. The influence of the microbiome on allergic sensitization to food. J Immunol Baltim Md. 1950;198:581–9.Google Scholar
  11. 11.
    Hansen CHF, Nielsen DS, Kverka M, Zakostelska Z, Klimesova K, Hudcovic T, Tlaskalova-Hogenova H, Hansen AK. Patterns of early gut colonization shape future immune responses of the host. PLoS One. 2012;7:e34043.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Hill DA, Siracusa MC, Abt MC, Kim BS, Kobuley D, Kubo M, et al. Commensal bacteria–derived signals regulate basophil hematopoiesis and allergic inflammation. Nat Med. 2012;18:538–46.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Rodriguez B, Prioult G, Bibiloni R, Nicolis I, Mercenier A, Butel M-J, Waligora-Dupriet A-J. Germ-free status and altered caecal subdominant microbiota are associated with a high susceptibility to cow’s milk allergy in mice. FEMS Microbiol Ecol. 2011;76:133–44.PubMedCrossRefGoogle Scholar
  14. 14.
    Sampson HA, O’Mahony L, Burks AW, Plaut M, Lack G, Akdis CA. Mechanisms of food allergy. J Allergy Clin Immunol. 2018;141:11–9.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Wannemuehler MJ, Kiyono H, Babb JL, Michalek SM, McGhee JR. Lipopolysaccharide (LPS) regulation of the immune response: LPS converts germfree mice to sensitivity to oral tolerance induction. J Immunol. 1982;129:959–65.PubMedGoogle Scholar
  16. 16.
    Bashir MEH, Louie S, Shi HN, Nagler-Anderson C. Toll-like receptor 4 signaling by intestinal microbes influences susceptibility to food allergy. J Immunol. 2004;172:6978–87.PubMedCrossRefGoogle Scholar
  17. 17.
    Vatanen T, Kostic AD, d’Hennezel E, Siljander H, Franzosa EA, Yassour M, et al. Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell. 2016;165:842–53.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Lotz M, Gütle D, Walther S, Ménard S, Bogdan C, Hornef MW. Postnatal acquisition of endotoxin tolerance in intestinal epithelial cells. J Exp Med. 2006;203:973–84.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Maynard CL, Elson CO, Hatton RD, Weaver CT. Reciprocal interactions of the intestinal microbiota and immune system. Nature. 2012;489(7415):231–41. Scholar
  20. 20.
    Kraj P, Ignatowicz L. The mechanisms shaping the repertoire of CD4+ Foxp3+ regulatory T cells. Immunology. 2018;153:290–6.PubMedCrossRefGoogle Scholar
  21. 21.
    Geuking MB, Cahenzli J, Lawson MAE, Ng DCK, Slack E, Hapfelmeier S, et al. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity. 2011;34:794–806.PubMedCrossRefGoogle Scholar
  22. 22.
    Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature. 2013;500:232–6.PubMedCrossRefGoogle Scholar
  23. 23.
    Skelly AN, Sato Y, Kearney S, Honda K. Mining the microbiota for microbial and metabolite-based immunotherapies. Nat Rev Immunol. 2019;19:305–23.PubMedCrossRefGoogle Scholar
  24. 24.
    Round JL, Lee SM, Li J, Tran G, Jabri B, Chatila TA, Mazmanian SK. The Toll-like receptor pathway establishes commensal gut colonization. Science. 2011;332:974–7.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Verma R, Lee C, Jeun E-J, Yi J, Kim KS, Ghosh A, et al. Cell surface polysaccharides of Bifidobacterium bifidum induce the generation of Foxp3+ regulatory T cells. Sci Immunol. 2018;3(28):pii: eaat6975. Scholar
  26. 26.
    Turcanu V, Brough HA, Toit GD, Foong R-X, Marrs T, Santos AF, Lack G. Immune mechanisms of food allergy and its prevention by early intervention. Curr Opin Immunol. 2017;48:92–8.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Barcik W, Wawrzyniak M, Akdis CA, O’Mahony L. Immune regulation by histamine and histamine-secreting bacteria. Curr Opin Immunol. 2017;48:108–13.PubMedCrossRefGoogle Scholar
  28. 28.
    Tan J, McKenzie C, Vuillermin PJ, Goverse G, Vinuesa CG, Mebius RE, et al. Dietary fiber and bacterial SCFA enhance oral tolerance and protect against food allergy through diverse cellular pathways. Cell Rep. 2016;15:2809–24.PubMedCrossRefGoogle Scholar
  29. 29.
    Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341:569–73.PubMedCrossRefGoogle Scholar
  30. 30.
    Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504:446–50.PubMedCrossRefGoogle Scholar
  31. 31.
    McKenzie C, Tan J, Macia L, Mackay CR. The nutrition-gut microbiome-physiology axis and allergic diseases. Immunol Rev. 2017;278:277–95.PubMedCrossRefGoogle Scholar
  32. 32.
    Hirata S-I, Kunisawa J. Gut microbiome, metabolome, and allergic diseases. Allergol Int Off J Jpn Soc Allergol. 2017;66:523–8.CrossRefGoogle Scholar
  33. 33.
    Shibata N, Kunisawa J, Kiyono H. Dietary and microbial metabolites in the regulation of host immunity. Front Microbiol. 2017;8:2171. Scholar
  34. 34.
    Kishino S, Takeuchi M, Park S-B, Hirata A, Kitamura N, Kunisawa J, et al. Polyunsaturated fatty acid saturation by gut lactic acid bacteria affecting host lipid composition. Proc Natl Acad Sci. 2013;110:17808–13.PubMedCrossRefGoogle Scholar
  35. 35.
    Kunisawa J, Arita M, Hayasaka T, Harada T, Iwamoto R, Nagasawa R, et al. Dietary ω3 fatty acid exerts anti-allergic effect through the conversion to 17,18-epoxyeicosatetraenoic acid in the gut. Sci Rep. 2015;5:9750.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Yates CM, Calder PC, Ed Rainger G. Pharmacology and therapeutics of omega-3 polyunsaturated fatty acids in chronic inflammatory disease. Pharmacol Ther. 2014;141:272–82.PubMedCrossRefGoogle Scholar
  37. 37.
    Kremmyda L-S, Vlachava M, Noakes PS, Diaper ND, Miles EA, Calder PC. Atopy risk in infants and children in relation to early exposure to fish, oily fish, or long-chain omega-3 fatty acids: a systematic review. Clin Rev Allergy Immunol. 2011;41:36–66.PubMedCrossRefGoogle Scholar
  38. 38.
    Gensollen T, Blumberg RS. Correlation between early-life regulation of the immune system by microbiota and allergy development. J Allergy Clin Immunol. 2017;139:1084–91.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Mueller NT, Bakacs E, Combellick J, Grigoryan Z, Dominguez-Bello MG. The infant microbiome development: mom matters. Trends Mol Med. 2015;21:109–17.PubMedCrossRefGoogle Scholar
  40. 40.
    Blaser MJ, Dominguez-Bello MG. The human microbiome before birth. Cell Host Microbe. 2016;20:558–60.PubMedCrossRefGoogle Scholar
  41. 41.
    Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med. 2014;6(237):237ra65. Scholar
  42. 42.
    Lauder AP, Roche AM, Sherrill-Mix S, Bailey A, Laughlin AL, Bittinger K, et al. Comparison of placenta samples with contamination controls does not provide evidence for a distinct placenta microbiota. Microbiome. 2016;4:29.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Leiby JS, McCormick K, Sherrill-Mix S, Clarke EL, Kessler LR, Taylor LJ, et al. Lack of detection of a human placenta microbiome in samples from preterm and term deliveries. Microbiome. 2018;6:196.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Moles L, Gomez M, Heilig H, Bustos G, Fuentes S, de Vos W, et al. Bacterial diversity in meconium of preterm neonates and evolution of their fecal microbiota during the first month of life. PLoS One. 2013;8:e66986.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Aidy SE, Hooiveld G, Tremaroli V, Bäckhed F, Kleerebezem M. The gut microbiota and mucosal homeostasis. Gut Microbes. 2013;4:118–24.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17:852.PubMedCrossRefGoogle Scholar
  47. 47.
    Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci. 2010;107:11971–5.PubMedCrossRefGoogle Scholar
  48. 48.
    Jakobsson HE, Abrahamsson TR, Jenmalm MC, Harris K, Quince C, Jernberg C, et al. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut. 2014;63:559–66.PubMedCrossRefGoogle Scholar
  49. 49.
    Thavagnanam S, Fleming J, Bromley A, Shields MD, Cardwell CR. A meta-analysis of the association between caesarean section and childhood asthma. Clin Exp Allergy. 2008;38:629–33.PubMedCrossRefGoogle Scholar
  50. 50.
    Lieberman JA, Greenhawt M, Nowak-Wegrzyn A. The environment and food allergy. Ann Allergy Asthma Immunol. 2018;120:455–7.PubMedCrossRefGoogle Scholar
  51. 51.
    Jost T, Lacroix C, Braegger CP, Rochat F, Chassard C. Vertical mother-neonate transfer of maternal gut bacteria via breastfeeding. Environ Microbiol. 2014;16:2891–904.PubMedCrossRefGoogle Scholar
  52. 52.
    Penders J, Vink C, Driessen C, London N, Thijs C, Stobberingh EE. Quantification of Bifidobacterium spp., Escherichia coli and Clostridium difficile in faecal samples of breast-fed and formula-fed infants by real-time PCR. FEMS Microbiol Lett. 2005;243(1):141–7.PubMedCrossRefGoogle Scholar
  53. 53.
    Azad MB, Becker AB, Guttman DS, Sears MR, Scott JA, Kozyrskyj AL. Gut microbiota diversity and atopic disease: does breast-feeding play a role? J Allergy Clin Immunol. 2013;131:247–8.PubMedCrossRefGoogle Scholar
  54. 54.
    Yasmin F, Tun HM, Konya TB, Guttman DS, Chari RS, Field CJ, et al. Cesarean section, formula feeding, and infant antibiotic exposure: separate and combined impacts on gut microbial changes in later infancy. Front Pediatr. 2017;5:200. eCollection 2017.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Lodge CJ, Tan DJ, Lau MXZ, Dai X, Tham R, Lowe AJ, et al. Breastfeeding and asthma and allergies: a systematic review and meta-analysis. Acta Paediatr. 2015;104:38–53.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Sonnenburg ED, Smits SA, Tikhonov M, Higginbottom SK, Wingreen NS, Sonnenburg JL. Diet-induced extinctions in the gut microbiota compound over generations. Nature. 2016;529:212–5.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Thorburn AN, McKenzie CI, Shen S, Stanley D, Macia L, Mason LJ, et al. Evidence that asthma is a developmental origin disease influenced by maternal diet and bacterial metabolites. Nat Commun. 2015;6:7320.PubMedCrossRefGoogle Scholar
  58. 58.
    Chu DM, Meyer KM, Prince AL, Aagaard KM. Impact of maternal nutrition in pregnancy and lactation on offspring gut microbial composition and function. Gut Microbes. 2016;7:459–70.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Sears MR, et al. Infant gut microbiota and the hygiene hypothesis of allergic disease: impact of household pets and siblings on microbiota composition and diversity. Allergy Asthma Clin Immunol Off J Can Soc Allergy Clin Immunol. 2013;9:15.CrossRefGoogle Scholar
  60. 60.
    Bufford JD, Reardon CL, Li Z, Roberg KA, DaSilva D, Eggleston PA, et al. Effects of dog ownership in early childhood on immune development and atopic diseases. Clin Exp Allergy. 2008;38(10):1635–43. Scholar
  61. 61.
    Ownby DR, Johnson CC, Peterson EL. Exposure to dogs and cats in the first year of life and risk of allergic sensitization at 6 to 7 years of age. JAMA. 2002;288:963–72.PubMedCrossRefGoogle Scholar
  62. 62.
    Tun HM, Konya T, Takaro TK, Brook JR, Chari R, Field CJ, et al. CHILD study investigators. Exposure to household furry pets influences the gut microbiota of infant at 3–4 months following various birth scenarios. Microbiome. 2017;5:40.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Ball TM, Castro-Rodriguez JA, Griffith KA, Holberg CJ, Martinez FD, Wright AL. Siblings, day-care attendance, and the risk of asthma and wheezing during childhood. N Engl J Med. 2000;343:538–43.PubMedCrossRefGoogle Scholar
  64. 64.
    Koplin JJ, Dharmage SC, Ponsonby A-L, Tang MLK, Lowe AJ, et al. HealthNuts investigators. Environmental and demographic risk factors for egg allergy in a population-based study of infants. Allergy. 2012;67:1415–22.PubMedCrossRefGoogle Scholar
  65. 65.
    Hesselmar B, Sjoberg F, Saalman R, Aberg N, Adlerberth I, Wold AE. Pacifier cleaning practices and risk of allergy development. Pediatrics. 2013;131:e1829–37.PubMedCrossRefGoogle Scholar
  66. 66.
    Hirsch AG, Pollak J, Glass TA, Poulsen MN, Bailey-Davis L, Mowery J, Schwartz BS. Early-life antibiotic use and subsequent diagnosis of food allergy and allergic diseases. Clin Exp Allergy J. 2017;47:236–44.CrossRefGoogle Scholar
  67. 67.
    Love BL, Mann JR, Hardin JW, Lu ZK, Cox C, Amrol DJ. Antibiotic prescription and food allergy in young children. Allergy Asthma Clin Immunol. 2016;12:41.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Bisgaard H, Li N, Bonnelykke K, Chawes BLK, Skov T, Paludan-Muller G, 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.e1–5.PubMedCrossRefGoogle Scholar
  69. 69.
    Berni Canani R, Sangwan N, Stefka AT, Nocerino R, Paparo L, Aitoro R, et al. Lactobacillus rhamnosus GG-supplemented formula expands butyrate-producing bacterial strains in food allergic infants. ISME J. 2016;10:742–50.PubMedCrossRefGoogle Scholar
  70. 70.
    Zhao W, Ho H-E, Bunyavanich S. The gut microbiome in food allergy. Ann Allergy Asthma Immunol. 2019;122(3):276–82. Scholar
  71. 71.
    Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer K-H, et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol. 2014;12:635–45.PubMedCrossRefGoogle Scholar
  72. 72.
    Weinstock GM. Genomic approaches to studying the human microbiota. Nature. 2012;489:250–6.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Azad MB, Konya T, Guttman DS, Field CJ, Sears MR, HayGlass KT, et al. CHILD study investigators. Infant gut microbiota and food sensitization: associations in the first year of life. Clin Exp Allergy J. 2015;45:632–43.CrossRefGoogle Scholar
  74. 74.
    Bunyavanich S, Shen N, Grishin A, Wood R, Burks W, Dawson P, Jet a. Early-life gut microbiome composition and milk allergy resolution. J Allergy Clin Immunol. 2016;138:1122–30.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Fazlollahi M, Chun Y, Grishin A, Wood RA, Burks AW, Dawson P, et al. Early-life gut microbiome and egg allergy. Allergy. 2018;73:1515–24.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Hua X, Goedert JJ, Pu A, Yu G, Shi J. Allergy associations with the adult fecal microbiota: analysis of the American gut project. EBioMedicine. 2016;3:172–9.PubMedCrossRefGoogle Scholar
  77. 77.
    Jackson MA, Verdi S, Maxan M-E, Shin CM, Zierer J, Bowyer RCE, et al. Gut microbiota associations with common diseases and prescription medications in a population-based cohort. Nat Commun. 2018;9:2655.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Noval Rivas M, Burton OT, Wise P, Zhang Y, Hobson SA, Garcia Lloret M, et al. A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis. J Allergy Clin Immunol. 2013;131:201–12.PubMedCrossRefGoogle Scholar
  79. 79.
    Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci. 2010;107:12204–9.PubMedCrossRefGoogle Scholar
  80. 80.
    Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 2011;331:337–41.PubMedCrossRefGoogle Scholar
  81. 81.
    Lopetuso LR, Scaldaferri F, Petito V, Gasbarrini A. Commensal Clostridia: leading players in the maintenance of gut homeostasis. Gut Pathog. 2013;5:23.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Chen C-C, Chen K-J, Kong M-S, Chang H-J, Huang J-L. Alterations in the gut microbiotas of children with food sensitization in early life. Pediatr Allergy Immunol. 2016;27:254–62.PubMedCrossRefGoogle Scholar
  83. 83.
    Stefka AT, Feehley T, Tripathi P, Qiu J, McCoy K, Mazmanian SK, et al. Commensal bacteria protect against food allergen sensitization. Proc Natl Acad Sci USA. 2014;111:13145–50.PubMedCrossRefGoogle Scholar
  84. 84.
    Feehley T, Plunkett CH, Bao R, Choi Hong SM, Culleen E, Belda-Ferre P, et al. Healthy infants harbor intestinal bacteria that protect against food allergy. Nat Med. 2019;25:448–53.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Bojanova DP, Bordenstein SR. Fecal transplants: what is being transferred? PLoS Biol. 2016;14:e1002503.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Grönlund M-M, Gueimonde M, Laitinen K, Kociubinski G, Grönroos T, Salminen S, Isolauri E. Maternal breast-milk and intestinal bifidobacteria guide the compositional development of the Bifidobacterium microbiota in infants at risk of allergic disease. Clin Exp Allergy J. 2007;37:1764–72.CrossRefGoogle Scholar
  87. 87.
    Garrido D, Dallas DC, Mills D. Consumption of human milk glycoconjugates by infant-associated bifidobacteria: mechanisms and implications. Microbiology. 2013;159(Pt 4):649–64. Epub 2013 Mar 4PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Lewis ZT, Mills DA. Differential establishment of bifidobacteria in the breastfed infant gut. Nestle Nutr Inst Workshop Ser. 2017;88:149–59.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Gigante G, Tortora A, Ianiro G, Ojetti V, Purchiaroni F, Campanale M, et al. Role of gut microbiota in food tolerance and allergies. Dig Dis Basel Switz. 2011;29:540–9.CrossRefGoogle Scholar
  90. 90.
    Garcia-Larsen V, Ierodiakonou D, Jarrold K, Cunha S, Chivinge J, Robinson Z, et al. Diet during pregnancy and infancy and risk of allergic or autoimmune disease: a systematic review and meta-analysis. PLoS Med. 2018;15:e1002507.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Wopereis H, Oozeer R, Knipping K, Belzer C, Knol J. The first thousand days – intestinal microbiology of early life: establishing a symbiosis. Pediatr Allergy Immunol. 2014;25:428–38.PubMedCrossRefGoogle Scholar
  92. 92.
    Grimshaw KEC, Maskell J, Oliver EM, Morris RCG, Foote KD, Mills ENC, et al. Diet and food allergy development during infancy: birth cohort study findings using prospective food diary data. J Allergy Clin Immunol. 2014;133:511–9.PubMedCrossRefGoogle Scholar
  93. 93.
    Venkataraman A, Sieber JR, Schmidt AW, Waldron C, Theis KR, Schmidt TM. Variable responses of human microbiomes to dietary supplementation with resistant starch. Microbiome. 2016;4:33.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Ciaccio CE, Girdhar M. Effect of maternal ω3 fatty acid supplementation on infant allergy. Ann Allergy Asthma Immunol. 2014;112:191–4.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Menni C, Zierer J, Pallister T, Jackson MA, Long T, Mohney RP, et al. Omega-3 fatty acids correlate with gut microbiome diversity and production of N-carbamylglutamate in middle aged and elderly women. Sci Rep. 2017;7:11079.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Watson H, Mitra S, Croden FC, Taylor M, Wood HM, Perry SL, et al. A randomised trial of the effect of omega-3 polyunsaturated fatty acid supplements on the human intestinal microbiota. Gut. 2018;67:1974–83.PubMedCrossRefGoogle Scholar
  97. 97.
    Vandenplas Y, De Greef E, Devreker T, Veereman-Wauters G, Hauser B. Probiotics and prebiotics in infants and children. Curr Infect Dis Rep. 2013;15:251–62.PubMedCrossRefGoogle Scholar
  98. 98.
    Bron PA, Kleerebezem M, Brummer R-J, Cani PD, Mercenier A, MacDonald TT, et al. Can probiotics modulate human disease by impacting intestinal barrier function? Br J Nutr. 2017;117:93–107.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    La Fata G, Weber P, Mohajeri MH. Probiotics and the gut immune system: indirect regulation. Probiotics Antimicrob Proteins. 2018;10:11–21.PubMedCrossRefGoogle Scholar
  100. 100.
    Ma N, Guo P, Zhang J, He T, Kim SW, Zhang G, Ma X. Nutrients mediate intestinal bacteria–mucosal immune crosstalk. Front Immunol. 2018;9:5. Scholar
  101. 101.
    Niers LEM, Timmerman HM, Rijkers GT, van Bleek GM, van Uden NOP, Knol EF, et al. Identification of strong interleukin-10 inducing lactic acid bacteria which down-regulate T helper type 2 cytokines. Clin Exp Allergy J Br Soc Allergy Clin Immunol. 2005;35:1481–9.CrossRefGoogle Scholar
  102. 102.
    Tang MLK, Ponsonby A-L, Orsini F, Tey D, Robinson M, Su EL, et al. Administration of a probiotic with peanut oral immunotherapy: a randomized trial. J Allergy Clin Immunol. 2015;135:737–744.e8.CrossRefGoogle Scholar
  103. 103.
    Tang R-B, Chang J-K, Chen H-L. Can probiotics be used to treat allergic diseases? J Chin Med Assoc JCMA. 2015;78:154–7.PubMedCrossRefGoogle Scholar
  104. 104.
    Benitez AJ, Hoffmann C, Muir AB, Dods KK, Spergel JM, Bushman FD, Wang M-L. Inflammation-associated microbiota in pediatric eosinophilic esophagitis. Microbiome. 2015;3:23.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Noti M, EDT W, Kim BS, Siracusa MC, Giacomin PR, Nair MG, et al. Thymic stromal lymphopoietin–elicited basophil responses promote eosinophilic esophagitis. Nat Med. 2013;19:1005–13.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Jensen ET, Kuhl JT, Martin LJ, Rothenberg ME, Dellon ES. Prenatal, intrapartum, and postnatal factors are associated with pediatric eosinophilic esophagitis. J Allergy Clin Immunol. 2018;141:214–22.PubMedCrossRefGoogle Scholar
  107. 107.
    Radano MC, Yuan Q, Katz A, Fleming JT, Kubala S, Shreffler W, Keet CA. Cesarean section and antibiotic use found to be associated with eosinophilic esophagitis. J Allergy Clin Immunol Pract. 2014;2:475–477.e1.PubMedCrossRefGoogle Scholar
  108. 108.
    Green DJ, Cotton CC, Dellon ES. The role of environmental exposures in the etiology of eosinophilic esophagitis: a systematic review. Mayo Clin Proc. 2015;90:1400–10.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Harris JK, Fang R, Wagner BD, Choe HN, Kelly CJ, Schroeder S, et al. Esophageal microbiome in eosinophilic esophagitis. PLoS One. 2015;10:e0128346.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Corning B, Copland AP, Frye JW. The esophageal microbiome in health and disease. Curr Gastroenterol Rep. 2018;20:39.PubMedCrossRefGoogle Scholar
  111. 111.
    Spechler SJ. Speculation as to why the frequency of eosinophilic esophagitis is increasing. Curr Gastroenterol Rep. 2018;20:26.PubMedCrossRefGoogle Scholar
  112. 112.
    Smith AR, Macfarlane S, Furrie E, Ahmed S, Bahrami B, Reynolds N, Macfarlane GT. Microbiological and immunological effects of enteral feeding on the upper gastrointestinal tract. J Med Microbiol. 2011;60:359–65.PubMedCrossRefGoogle Scholar
  113. 113.
    Schneider S-M. Microbiota and enteral nutrition. Gastroentérologie Clin Biol. 2010;34:S57–61.CrossRefGoogle Scholar
  114. 114.
    Walton C, Montoya MPB, Fowler DP, Turner C, Jia W, Whitehead RN, et al. Enteral feeding reduces metabolic activity of the intestinal microbiome in Crohn’s disease: an observational study. Eur J Clin Nutr. 2016;70:1052–6.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Alyson L. Yee
    • 1
  • Mary M. Buschmann
    • 2
  • Christina E. Ciaccio
    • 3
  • Jack A. Gilbert
    • 2
  1. 1.Interdisciplinary Scientist Training Program, University of ChicagoChicagoUSA
  2. 2.Department of Pediatrics and Scripps Institution of OceanographyUniversity of California San DiegoLa JollaUSA
  3. 3.Department of Pediatrics and MedicineThe University of ChicagoChicagoUSA

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