Skip to main content

Advertisement

Log in

Role of the Microbiome in Allergic Disease Development

  • Allergies and the Environment (T Moran, Section Editor)
  • Published:
Current Allergy and Asthma Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

Evidence suggests that the microbiome of the skin, gastrointestinal tract, and airway contribute to health and disease. As we learn more about the role that the microbiota plays in allergic disease development, we can develop therapeutics to alter this pathway.

Recent Findings

Epidemiologic studies reveal that an association exists between environmental exposures, which alter the microbiota, and developing atopic dermatitis, food allergy, and/or asthma. In fact, samples from the skin, gastrointestinal tract, and respiratory tract reveal distinct microbiotas compared with healthy controls, with microbial changes (dysbiosis) often preceding the development of allergic disease. Mechanistic studies have confirmed that microbes can either promote skin, gut, and airway health by strengthening barrier integrity, or they can alter skin integrity and damage gut and airway epithelium.

Summary

In this review, we will discuss recent studies that reveal the link between the microbiota and immune development, and we will discuss ways to influence these changes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: •• Of major importance

  1. Shu SA, Yuen AWT, Woo E, Chu KH, Kwan HS, Yang GX, et al. Microbiota and food allergy. Clin Rev Allergy Immunol. 2019;57(1):83–97.

    CAS  PubMed  Google Scholar 

  2. Marrs T, Sim K. Demystifying dysbiosis: can the gut microbiome promote oral tolerance over IgE-mediated food allergy? Curr Pediatr Rev. 2018;14(3):156–63.

    CAS  PubMed  Google Scholar 

  3. Cukrowska B. Microbial and nutritional programming-the importance of the microbiome and early exposure to potential food allergens in the development of allergies. Nutrients. 2018;10(10):18.

    Google Scholar 

  4. Bunyavanich B. Food allergy and the microbiome: current understandings and future directions. J Allergy Clin Immunol. 2019;144(6):1468–77.

    PubMed  PubMed Central  Google Scholar 

  5. Zoe C, KAW S, Pamela A. Frischmeyer-Guerrerio. Recent developments in understanding the mechanisms of food allergy. Wolters Kluwer Health. 2019;21:6.

    Google Scholar 

  6. Oh J, Byrd AL, Deming C, Conlan S, Program NCS, Kong HH, et al. Biogeography and individuality shape function in the human skin metagenome. Nature. 2014;514(7520):59–64.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Findley K, Oh J, Yang J, Conlan S, Deming C, Meyer JA, et al. Topographic diversity of fungal and bacterial communities in human skin. Nature. 2013;498(7454):367–70.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Lunjani N, Satitsuksanoa P, Lukasik Z, Sokolowska M, Eiwegger T, O'Mahony L. Recent developments and highlights in mechanisms of allergic diseases: microbiome. Allergy. 2018;73(12):2314–27.

    PubMed  Google Scholar 

  9. Fieten KB, Totte JEE, Levin E, Reyman M, Meijer Y, Knulst A, et al. Fecal microbiome and food allergy in pediatric atopic dermatitis: a cross-sectional pilot study. Int Arch Allergy Immunol. 2018;175(1–2):77–84.

    CAS  PubMed  Google Scholar 

  10. Jensen-Jarolim E, Pali-Scholl I, Roth-Walter F. Outstanding animal studies in allergy II. From atopic barrier and microbiome to allergen-specific immunotherapy. Curr Opin Allergy Clin Immunol. 2017;17(3):180–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Ramsey MM, Freire MO, Gabrilska RA, Rumbaugh KP, Lemon KP. Staphylococcus aureus shifts toward commensalism in response to Corynebacterium species. Front Microbiol. 2016;7:1230.

    PubMed  PubMed Central  Google Scholar 

  12. Kong HH, Oh J, Deming C, Conlan S, Grice EA, Beatson MA, et al. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res. 2012;22(5):850–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Fyhrquist N, Ruokolainen L, Suomalainen A, Lehtimaki S, Veckman V, Vendelin J, et al. Acinetobacter species in the skin microbiota protect against allergic sensitization and inflammation. J Allergy Clin Immunol. 2014;134(6):1301–9 e11.

    CAS  PubMed  Google Scholar 

  14. Sugimoto S, Iwamoto T, Takada K, Okuda K, Tajima A, Iwase T, et al. Staphylococcus epidermidis Esp degrades specific proteins associated with Staphylococcus aureus biofilm formation and host-pathogen interaction. J Bacteriol. 2013;195(8):1645–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Meylan P, Lang C, Mermoud S, Johannsen A, Norrenberg S, Hohl D, et al. Skin colonization by Staphylococcus aureus precedes the clinical diagnosis of atopic dermatitis in infancy. J Invest Dermatol. 2017;137(12):2497–504.

    CAS  PubMed  Google Scholar 

  16. Kennedy EA, Connolly J, Hourihane JO, Fallon PG, McLean WHI, Murray D, 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. J Allergy Clin Immunol. 2017;139(1):166–72.

    PubMed  PubMed Central  Google Scholar 

  17. Nakamura Y, Oscherwitz J, Cease KB, Chan SM, Munoz-Planillo R, Hasegawa M, et al. Staphylococcus delta-toxin induces allergic skin disease by activating mast cells. Nature. 2013;503(7476):397–401.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. •• Tauber M, Balica S, Hsu CY, Jean-Decoster C, Lauze C, Redoules D, et al. Staphylococcus aureus density on lesional and nonlesional skin is strongly associated with disease severity in atopic dermatitis. J Allergy Clin Immunol. 2016;137(4):1272–4 e3. Staphylococcus aureusabundance increases during skin flares. Increased abundance ofS. aureusis associated with increased severity of atopic dermatitis.

    PubMed  Google Scholar 

  19. Kemter AM, Nagler CR. Influences on allergic mechanisms through gut, lung, and skin microbiome exposures. J Clin Invest. 2019;130:1483–92.

    Google Scholar 

  20. Nakatsuji T, Chen TH, Two AM, Chun KA, Narala S, Geha RS, et al. Staphylococcus aureus exploits epidermal barrier defects in atopic dermatitis to trigger cytokine expression. J Invest Dermatol. 2016;136(11):2192–200.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Hirasawa Y, Takai T, Nakamura T, Mitsuishi K, Gunawan H, Suto H, et al. Staphylococcus aureus extracellular protease causes epidermal barrier dysfunction. J Invest Dermatol. 2010;130(2):614–7.

    CAS  PubMed  Google Scholar 

  22. Iwamoto K, Numm TJ, Koch S, Herrmann N, Leib N, Bieber T. Langerhans and inflammatory dendritic epidermal cells in atopic dermatitis are tolerized toward TLR2 activation. Allergy. 2018;73(11):2205–13.

    CAS  PubMed  Google Scholar 

  23. Seite S, Bieber T. Barrier function and microbiotic dysbiosis in atopic dermatitis. Clin Cosmet Investig Dermatol. 2015;8:479–83.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Geoghegan JA, Dufrene YF. Mechanomicrobiology: how mechanical forces activate Staphylococcus aureus adhesion. Trends Microbiol. 2018;26(8):645–8.

    CAS  PubMed  Google Scholar 

  25. Di Domenico EG, Cavallo I, Capitanio B, Ascenzioni F, Pimpinelli F, Morrone A, et al. Staphylococcus aureus and the cutaneous microbiota biofilms in the pathogenesis of atopic dermatitis. Microorganisms. 2019;7:9.

  26. Thomas CL, Fernandez-Penas P. The microbiome and atopic eczema: more than skin deep. Australas J Dermatol. 2017;58(1):18–24.

    PubMed  Google Scholar 

  27. Penders J, Thijs C, van den Brandt PA, Kummeling I, Snijders B, Stelma F, et al. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study. Gut. 2007;56(5):661–7.

    CAS  PubMed  Google Scholar 

  28. Abrahamsson TR, Jakobsson HE, Andersson AF, Bjorksten B, Engstrand L, Jenmalm MC. Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol. 2012;129(2):434–40, 40 e1–2.

    PubMed  Google Scholar 

  29. Lee MJ, Kang MJ, Lee SY, Lee E, Kim K, Won S, et al. Perturbations of gut microbiome genes in infants with atopic dermatitis according to feeding type. J Allergy Clin Immunol. 2018;141(4):1310–9.

    CAS  PubMed  Google Scholar 

  30. Watanabe S, Narisawa Y, Arase S, Okamatsu H, Ikenaga T, Tajiri Y, et al. Differences in fecal microflora between patients with atopic dermatitis and healthy control subjects. J Allergy Clin Immunol. 2003;111(3):587–91.

    PubMed  Google Scholar 

  31. Myles IAEN, Anderson ED, et al. First-in-human topical microbiome transplantation with Roseomonas mucosa for atopic dermatitis. JCI Insight. 2018;3.

  32. Nakatsuji TCT, Narala S, et al. Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis. Sci Transl Med. 2017:9.

  33. Tadao Enomoto MS, Nishimori K, Shimazu S, Yoshida A, Yamada K, Furukawa F, et al. Effects of bifidobacterial supplementation to pregnant women and infants in the prevention of allergy development in infants and on fecal microbiota. Allergol Int. 2014;63(4):575–85.

    PubMed  Google Scholar 

  34. Chernikova D, Yuan I, Shaker M. Prevention of allergy with diverse and healthy microbiota: an update. Curr Opin Pediatr. 2019;31(3):418–25.

    PubMed  Google Scholar 

  35. Dotterud CK, OS, Johnsen R, Oien T. Probiotics in pregnant women to prevent allergic disease: a randomized, double-blind trial. Br J Dermato. 2010;163(3):616–23.

    CAS  Google Scholar 

  36. Cabana MDMM, Caughey AB, et al. Early probiotic supplementation for eczema and asthma prevention: a randomized controlled trial. Pediatrics. 2017;140:3.

    Google Scholar 

  37. Backhed 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(6):852.

    CAS  PubMed  Google Scholar 

  38. Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118(2):511–21.

    PubMed  Google Scholar 

  39. Gronlund MM, Lehtonen OP, Eerola E, Kero P. Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. J Pediatr Gastroenterol Nutr. 1999;28(1):19–25.

    CAS  PubMed  Google Scholar 

  40. Kalliomaki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin Immunol. 2001;107(1):129–34.

    CAS  PubMed  Google Scholar 

  41. Bunyavanich S. Food allergy: could the gut microbiota hold the key? Nat Rev Gastroenterol Hepatol. 2019;16(4):201–2.

    PubMed  Google Scholar 

  42. Bisgaard H, LN, Bonnelykke K, Chawes BL, Skov T, Paudan-Müller 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.e5.

    PubMed  Google Scholar 

  43. Sjogren YM, Jenmalm MC, Bottcher MF, Bjorksten B, Sverremark-Ekstrom E. Altered early infant gut microbiota in children developing allergy up to 5 years of age. Clin Exp Allergy. 2009;39(4):518–26.

    CAS  PubMed  Google Scholar 

  44. Hayen SM, den Hartog Jager CF, Knulst AC, Knol EF, Garssen J, Willemsen LEM, et al. Non-digestible oligosaccharides can suppress basophil degranulation in whole blood of peanut-allergic patients. Front Immunol. 2018;9:1265.

    PubMed  PubMed Central  Google Scholar 

  45. Roger LC, Costabile A, Holland DT, Hoyles L, McCartney AL. Examination of faecal Bifidobacterium populations in breast- and formula-fed infants during the first 18 months of life. Microbiology. 2010;156(Pt 11):3329–41.

    CAS  PubMed  Google Scholar 

  46. •• Peter J, MOH V, Collier F, Allen KJ, Tang MLK, Harrison LC, et al. Maternal carriage of Prevotella during pregnancy associates with protection against food allergy in the offspring. Nat Commun. 2020;11:1452. Nested case-cohort study revealing maternal carriage of Prevotella copri in stool during pregnancy was strongly associated with the absence of food allergy development in offspring.

    Google Scholar 

  47. Tracy J. Pitt ABB, Moira Chan-Yeung, Edmond S. Chan, Wade T. A. Watson, Rishma Chooniedass, Meghan B. Azad. Reduced risk of peanut sensitization following exposure through breast-feeding and early peanut introduction. Journal of Allergy & Clinical Immunology. 2017.

  48. Sicherer S. Maternal consumption of peanut during pregnancy is associated with peanut sensitization in atopic infants. J Allergy Clin Immunol. 2010;126:6.

    Google Scholar 

  49. Carina Venter PhD KMP, John W. Holloway PhD, Lori J. Silveira PhD, David M. Fleischer MD, Taraneh Dean PhD,S. Hasan Arshad MD. Different measures of diet diversity during infancy and the association with childhood food allergy in a UK birth cohort study Journal of Allergy & Clinical Immunology. 2020.

  50. Paola Musso EC, Roberto Bernardini. Human microbiome and allergic diseases in children: pathogenetic role and therapeutic options. Curr Pediatr Rev 2019;15.

  51. •• George Du Toit GR, Sayre PH, Bahnson HT, Radulovic S, Santos AF, Brough HA, et al. Randomized trial of peanut consumption in infants at risk for peanut allergy. N Engl J Med. 2015;372:9. Early introduction of peanut significantly decreased the frequency of developing peanut allergy in a high-risk infant cohort.

    Google Scholar 

  52. Caroline Roduit RF, Depner M, Schaub B, Loss G, Genuneit J, Pfefferle P, et al. Increased food diversity in the first year of life is inversely associated with allergic diseases. J Allergy Clin Immunol. 2014;133(4):1056–64.

    PubMed  Google Scholar 

  53. du Toit G, Sayre PH, Roberts G, Lawson K, Sever ML, Bahnson HT, et al. Allergen specificity of early peanut consumption and effect on development of allergic disease in the Learning Early About Peanut Allergy study cohort. J Allergy Clin Immunol. 2018;141(4):1343–53.

    PubMed  Google Scholar 

  54. Yassour M, Vatanen T, Siljander H, Hamalainen AM, Harkonen T, Ryhanen SJ, et al. Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability. Sci Transl Med. 2016;8(343):343ra81.

    PubMed  PubMed Central  Google Scholar 

  55. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486(7402):222–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Fazlollahi M, Chun Y, Grishin A, Wood RA, Burks AW, Dawson P, et al. Early-life gut microbiome and egg allergy. Allergy. 2018;73(7):1515–24.

    CAS  PubMed  Google Scholar 

  57. 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(3):742–50.

    CAS  PubMed  Google Scholar 

  58. Bunyavanich S, Shen N, Grishin A, Wood R, Burks W, Dawson P, et al. Early-life gut microbiome composition and milk allergy resolution. J Allergy Clin Immunol. 2016;138(4):1122–30.

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Lathrop SK, Bloom SM, Rao SM, Nutsch K, Lio CW, Santacruz N, et al. Peripheral education of the immune system by colonic commensal microbiota. Nature. 2011;478(7368):250–4.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Geuking MB, Cahenzli J, Lawson MA, Ng DC, Slack E, Hapfelmeier S, et al. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity. 2011;34(5):794–806.

    CAS  PubMed  Google Scholar 

  61. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504(7480):451–455.

  62. 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(7480):446–50.

    CAS  PubMed  Google Scholar 

  63. 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(12):2809–24.

    CAS  PubMed  Google Scholar 

  64. Berni Canani R, Di Costanzo M, Bedogni G, Amoroso A, Cosenza L, Di Scala C, et al. Extensively hydrolyzed casein formula containing Lactobacillus rhamnosus GG reduces the occurrence of other allergic manifestations in children with cow's milk allergy: 3-year randomized controlled trial. J Allergy Clin Immunol. 2017;139(6):1906–13 e4.

    CAS  PubMed  Google Scholar 

  65. Tang ML, Ponsonby AL, 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(3):737–44 e8.

    CAS  PubMed  Google Scholar 

  66. Cuello-Garcia CA, Brozek JL, Fiocchi A, Pawankar R, Yepes-Nunez JJ, Terracciano L, et al. Probiotics for the prevention of allergy: a systematic review and meta-analysis of randomized controlled trials. J Allergy Clin Immunol. 2015;136(4):952–61.

    PubMed  Google Scholar 

  67. Fiocchi A, Pawankar R, Cuello-Garcia C, Ahn K, Al-Hammadi S, Agarwal A, et al. World Allergy Organization-McMaster University Guidelines for Allergic Disease Prevention (GLAD-P): probiotics. World Allergy Organ J. 2015;8(1):4.

    PubMed  PubMed Central  Google Scholar 

  68. Zhao W, Ho HE, Bunyavanich S. The gut microbiome in food allergy. Ann Allergy Asthma Immunol. 2019;122(3):276–82.

    CAS  PubMed  Google Scholar 

  69. van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368(5):407–15.

    PubMed  Google Scholar 

  70. Youngster I, Russell GH, Pindar C, Ziv-Baran T, Sauk J, Hohmann EL. Oral, capsulized, frozen fecal microbiota transplantation for relapsing Clostridium difficile infection. JAMA. 2014;312(17):1772–8.

    CAS  PubMed  Google Scholar 

  71. Bisgaard H, Hermansen MN, Buchvald F, Loland L, Halkjaer LB, Bonnelykke K, et al. Childhood asthma after bacterial colonization of the airway in neonates. N Engl J Med. 2007;357(15):1487–95.

    CAS  PubMed  Google Scholar 

  72. Bisgaard H, Hermansen MN, Bonnelykke K, Stokholm J, Baty F, Skytt NL, et al. Association of bacteria and viruses with wheezy episodes in young children: prospective birth cohort study. Bmj. 2010;341:c4978.

    PubMed  PubMed Central  Google Scholar 

  73. Stein MM, Hrusch CL, Gozdz J, Igartua C, Pivniouk V, Murray SE, et al. Innate immunity and asthma risk in Amish and Hutterite farm children. N Engl J Med. 2016;375(5):411–21.

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Schuijs MJ, Willart MA, Vergote K, Gras D, Deswarte K, Ege MJ, et al. Farm dust and endotoxin protect against allergy through A20 induction in lung epithelial cells. Science. 2015;349(6252):1106–10.

    CAS  PubMed  Google Scholar 

  75. Kirjavainen PV, Karvonen AM, Adams RI, Taubel M, Roponen M, Tuoresmaki P, et al. Farm-like indoor microbiota in non-farm homes protects children from asthma development. Nat Med. 2019;25(7):1089–95.

    CAS  PubMed  Google Scholar 

  76. Holbreich M, Genuneit J, Weber J, Braun-Fahrlander C, Waser M, von Mutius E. Amish children living in northern Indiana have a very low prevalence of allergic sensitization. J Allergy Clin Immunol. 2012;129(6):1671–3.

    PubMed  Google Scholar 

  77. Ege MJ, Mayer M, Normand AC, Genuneit J, Cookson WO, Braun-Fahrlander C, et al. Exposure to environmental microorganisms and childhood asthma. N Engl J Med. 2011;364(8):701–9.

    CAS  PubMed  Google Scholar 

  78. Ege MJ, Frei R, Bieli C, Schram-Bijkerk D, Waser M, Benz MR, et al. Not all farming environments protect against the development of asthma and wheeze in children. J Allergy Clin Immunol. 2007;119(5):1140–7.

    PubMed  Google Scholar 

  79. Braun-Fahrlander C, Riedler J, Herz U, Eder W, Waser M, Grize L, et al. Environmental exposure to endotoxin and its relation to asthma in school-age children. N Engl J Med. 2002;347(12):869–77.

    PubMed  Google Scholar 

  80. Waser M, Michels KB, Bieli C, Floistrup H, Pershagen G, von Mutius E, et al. Inverse association of farm milk consumption with asthma and allergy in rural and suburban populations across Europe. Clin Exp Allergy. 2007;37(5):661–70.

    CAS  PubMed  Google Scholar 

  81. Darabi B, Rahmati S, HafeziAhmadi MR, Badfar G, Azami M. The association between caesarean section and childhood asthma: an updated systematic review and meta-analysis. Allergy, Asthma Clin Immunol. 2019;15:62.

    Google Scholar 

  82. Chu DM, Ma J, Prince AL, Antony KM, Seferovic MD, Aagaard KM. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat Med. 2017;23(3):314–26.

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Bosch A, Levin E, van Houten MA, Hasrat R, Kalkman G, Biesbroek G, et al. Development of upper respiratory tract microbiota in infancy is affected by mode of delivery. EBioMedicine. 2016;9:336–45.

    PubMed  PubMed Central  Google Scholar 

  84. Reyman M, van Houten MA, van Baarle D, Bosch A, Man WH, Chu M, et al. Impact of delivery mode-associated gut microbiota dynamics on health in the first year of life. Nat Commun. 2019;10(1):4997.

    PubMed  PubMed Central  Google Scholar 

  85. Duijts L, Jaddoe VW, Hofman A, Moll HA. Prolonged and exclusive breastfeeding reduces the risk of infectious diseases in infancy. Pediatrics. 2010;126(1):e18–25.

    PubMed  Google Scholar 

  86. Lopez-Alarcon M, Villalpando S, Fajardo A. Breast-feeding lowers the frequency and duration of acute respiratory infection and diarrhea in infants under six months of age. J Nutr. 1997;127(3):436–43.

    CAS  PubMed  Google Scholar 

  87. Paricio Talayero JM, Lizan-Garcia M, Otero Puime A, Benlloch Muncharaz MJ, Beseler Soto B, Sanchez-Palomares M, et al. Full breastfeeding and hospitalization as a result of infections in the first year of life. Pediatrics. 2006;118(1):e92–9.

    PubMed  Google Scholar 

  88. Tarrant M, Kwok MK, Lam TH, Leung GM, Schooling CM. Breast-feeding and childhood hospitalizations for infections. Epidemiology. 2010;21(6):847–54.

    PubMed  Google Scholar 

  89. Azad MB, Vehling L, Lu Z, Dai D, Subbarao P, Becker AB, et al. Breastfeeding, maternal asthma and wheezing in the first year of life: a longitudinal birth cohort study. Eur Respir J. 2017;49:5.

    Google Scholar 

  90. Bosch A, de Steenhuijsen Piters WAA, van Houten MA, Chu M, Biesbroek G, Kool J, et al. Maturation of the infant respiratory microbiota, environmental drivers, and health consequences. A prospective cohort study. Am J Respir Crit Care Med. 2017;196(12):1582–90.

    PubMed  Google Scholar 

  91. Biesbroek G, Tsivtsivadze E, Sanders EA, Montijn R, Veenhoven RH, Keijser BJ, et al. Early respiratory microbiota composition determines bacterial succession patterns and respiratory health in children. Am J Respir Crit Care Med. 2014;190(11):1283–92.

    PubMed  Google Scholar 

  92. Biesbroek G, Bosch AA, Wang X, Keijser BJ, Veenhoven RH, Sanders EA, et al. The impact of breastfeeding on nasopharyngeal microbial communities in infants. Am J Respir Crit Care Med. 2014;190(3):298–308.

    PubMed  Google Scholar 

  93. Teo SM, Mok D, Pham K, Kusel M, Serralha M, Troy N, et al. The infant nasopharyngeal microbiome impacts severity of lower respiratory infection and risk of asthma development. Cell Host Microbe. 2015;17(5):704–15.

    CAS  PubMed  PubMed Central  Google Scholar 

  94. McCauley K, Durack J, Valladares R, Fadrosh DW, Lin DL, Calatroni A, et al. Distinct nasal airway bacterial microbiotas differentially relate to exacerbation in pediatric patients with asthma. J Allergy Clin Immunol. 2019;144(5):1187–97.

    PubMed  PubMed Central  Google Scholar 

  95. •• Teo SM, HHF T, Mok D, Judd LM, Watts SC, Pham K, et al. Airway Microbiota Dynamics Uncover a Critical Window for Interplay of Pathogenic Bacteria and Allergy in Childhood Respiratory Disease. Cell Host Microbe. 2018;24(3):341–52.e5. This study demonstrates that asymptomatic colonization of the nasopharynx in early sensitized children withStreptococcus, Haemophilus,andMoraxella,increases the risk of persistent wheeze at 5 years of age.

  96. Hyde ER, Petrosino JF, Piedra PA, Camargo CA Jr, Espinola JA, Mansbach JM. Nasopharyngeal Proteobacteria are associated with viral etiology and acute wheezing in children with severe bronchiolitis. J Allergy Clin Immunol. 2014;133(4):1220–2.

    PubMed  Google Scholar 

  97. Rosas-Salazar C, Shilts MH, Tovchigrechko A, Schobel S, Chappell JD, Larkin EK, et al. Differences in the nasopharyngeal microbiome during acute respiratory tract infection with human rhinovirus and respiratory syncytial virus in infancy. J Infect Dis. 2016;214(12):1924–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Caliskan M, Bochkov YA, Kreiner-Moller E, Bonnelykke K, Stein MM, Du G, et al. Rhinovirus wheezing illness and genetic risk of childhood-onset asthma. N Engl J Med. 2013;368(15):1398–407.

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Rosas-Salazar C, Shilts MH, Tovchigrechko A, Schobel S, Chappell JD, Larkin EK, et al. Nasopharyngeal Lactobacillus is associated with a reduced risk of childhood wheezing illnesses following acute respiratory syncytial virus infection in infancy. J Allergy Clin Immunol. 2018;142(5):1447–56.e9.

    PubMed  PubMed Central  Google Scholar 

  100. •• Chun Y, Do A, Grishina G, Grishin A, Fang G, Rose S, et al. Integrative study of the upper and lower airway microbiome and transcriptome in asthma. JCI Insight. 2020;5(5). This study links the microbiome and transcriptome in asthmatic versus healthy children. Corynebacterium in the nasal microbiome shows negative associations with many genes related to inflammation in healthy children. This protective effect was attenuated in children with severe persistent asthma.

  101. Kloepfer KM, Sarsani VK, Poroyko V, Lee WM, Pappas TE, Kang T, et al. Community-acquired rhinovirus infection is associated with changes in the airway microbiome. J Allergy Clin Immunol. 2017;140(1):312–5 e8.

    PubMed  PubMed Central  Google Scholar 

  102. Hassan F, Ren D, Zhang W, Merkel TJ, Gu XX. Moraxella catarrhalis activates murine macrophages through multiple toll like receptors and has reduced clearance in lungs from TLR4 mutant mice. PLoS One. 2012;7(5):e37610.

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Alnahas S, Hagner S, Raifer H, Kilic A, Gasteiger G, Mutters R, et al. IL-17 and TNF-alpha are key mediators of Moraxella catarrhalis triggered exacerbation of allergic airway inflammation. Front Immunol. 2017;8:1562.

    PubMed  PubMed Central  Google Scholar 

  104. Gollwitzer ES, Saglani S, Trompette A, Yadava K, Sherburn R, McCoy KD, et al. Lung microbiota promotes tolerance to allergens in neonates via PD-L1. Nat Med. 2014;20(6):642–7.

    CAS  PubMed  Google Scholar 

  105. Forsythe P, Inman MD, Bienenstock J. Oral treatment with live Lactobacillus reuteri inhibits the allergic airway response in mice. Am J Respir Crit Care Med. 2007;175(6):561–9.

    PubMed  Google Scholar 

  106. Hjelmso MH, Shah SA, Thorsen J, Rasmussen M, Vestergaard G, Mortensen MS, et al. Prenatal dietary supplements influence the infant airway microbiota in a randomized factorial clinical trial. Nat Commun. 2020;11(1):426.

    PubMed  PubMed Central  Google Scholar 

Download references

Funding

The following grants supported this research:

1. National Institute of Allergy and Infectious Disease (NIAID) K23 Career development Award 1 K23 AI135094-01

2. American Academy of Allergy, Asthma and Immunology (AAAAI) Foundation Faculty Development Award

3. National Institute of Health Loan Repayment Program L40 AI096442

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kirsten M. Kloepfer.

Ethics declarations

Conflict of Interest

The authors declare no conflicts of interest relevant to this manuscript.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection on Allergies and the Environment

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aguilera, A.C., Dagher, I.A. & Kloepfer, K.M. Role of the Microbiome in Allergic Disease Development. Curr Allergy Asthma Rep 20, 44 (2020). https://doi.org/10.1007/s11882-020-00944-2

Download citation

  • Published:

  • DOI: https://doi.org/10.1007/s11882-020-00944-2

Keywords

Navigation