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Journal of Pediatric Biochemistry 2015; 05(02): 071-076
DOI: 10.1055/s-0035-1564578
Review Article
Georg Thieme Verlag KG Stuttgart · New York

Asthma, Atopy, and Intestinal Microbiota

Eishika Dissanayake
1   Department of Pediatrics, Graduate School of Medicine, Chiba University, Chiba, Japan
,
Naoki Shimojo
1   Department of Pediatrics, Graduate School of Medicine, Chiba University, Chiba, Japan
› Author Affiliations
Further Information

Publication History

22 July 2015

31 July 2015

Publication Date:
17 September 2015 (online)

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Abstract

Allergic diseases are on the rise and many studies have shown the differences in the gut microbiota among children with and without. The mode of delivery, breastfeeding, and antibiotic use during childhood have been strongly implicated as factors driving the early colonization and composition of the gut microbiome. It has been suggested that the reduced exposure to microbes during childhood causes an aberrance in the gut microbiome which prevents shift from T helper 2 cell (Th2) to T helper 1 cell (Th1)/regulatory T cell (Treg) response to maintain immune balance. Probiotics, prebiotics, and synbiotics are being studied as prospective interventions that can be used during pregnancy and infancy to prevent the development of allergic diseases later on in life. This review looks at the current knowledge on the role of the aberrant microbiome in the development of allergic diseases and how it can be modified for their prevention and treatment.

Keywords

allergic diseases - gut microbiome - probiotics - prebiotics
 

  • References

  • 1 Prescott SL. Early-life environmental determinants of allergic diseases and the wider pandemic of inflammatory noncommunicable diseases. J Allergy Clin Immunol 2013; 131 (1) 23-30
    CrossrefPubMedGoogle Scholar
  • 2 Shaker M. New insights into the allergic march. Curr Opin Pediatr 2014; 26 (4) 516-520
    CrossrefPubMedGoogle Scholar
  • 3 Dominguez-Bello MG, Costello EK, Contreras M , et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 2010; 107 (26) 11971-11975
    CrossrefPubMedGoogle Scholar
  • 4 Rautava S, Luoto R, Salminen S, Isolauri E. Microbial contact during pregnancy, intestinal colonization and human disease. Nat Rev Gastroenterol Hepatol 2012; 9 (10) 565-576
    CrossrefPubMedGoogle Scholar
  • 5 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
    CrossrefPubMedGoogle Scholar
  • 6 Stout MJ, Conlon B, Landeau M , et al. Identification of intracellular bacteria in the basal plate of the human placenta in term and preterm gestations. Am J Obstet Gynecol 2013; 208 (3) 226.e1-226.e7
    CrossrefPubMedGoogle Scholar
  • 7 Satokari R, Grönroos T, Laitinen K, Salminen S, Isolauri E. Bifidobacterium and Lactobacillus DNA in the human placenta. Lett Appl Microbiol 2009; 48 (1) 8-12
    CrossrefPubMedGoogle Scholar
  • 8 Abrahamsson TR, Wu RY, Jenmalm MC. Gut microbiota and allergy: the importance of the pregnancy period. Pediatr Res 2015; 77 (1–2) 214-219
    CrossrefPubMedGoogle Scholar
  • 9 Alm B, Erdes L, Möllborg P , et al. Neonatal antibiotic treatment is a risk factor for early wheezing. Pediatrics 2008; 121 (4) 697-702
    CrossrefPubMedGoogle Scholar
  • 10 Bager P, Wohlfahrt J, Westergaard T. Caesarean delivery and risk of atopy and allergic disease: meta-analyses. Clin Exp Allergy 2008; 38 (4) 634-642
    CrossrefPubMedGoogle Scholar
  • 11 Nwaru BI, Takkinen HM, Kaila M , et al. Food diversity in infancy and the risk of childhood asthma and allergies. J Allergy Clin Immunol 2014; 133 (4) 1084-1091
    CrossrefPubMedGoogle Scholar
  • 12 Ege MJ, Mayer M, Normand AC , et al; GABRIELA Transregio 22 Study Group. Exposure to environmental microorganisms and childhood asthma. N Engl J Med 2011; 364 (8) 701-709
    CrossrefPubMedGoogle Scholar
  • 13 Sjögren YM, Jenmalm MC, Böttcher MF, Björkstén B, Sverremark-Ekström E. Altered early infant gut microbiota in children developing allergy up to 5 years of age. Clin Exp Allergy 2009; 39 (4) 518-526
    CrossrefPubMedGoogle Scholar
  • 14 Hanski I, von Hertzen L, Fyhrquist N , et al. Environmental biodiversity, human microbiota, and allergy are interrelated. Proc Natl Acad Sci U S A 2012; 109 (21) 8334-8339
    CrossrefPubMedGoogle Scholar
  • 15 Song SJ, Lauber C, Costello EK , et al. Cohabiting family members share microbiota with one another and with their dogs. eLife 2013; 2: e00458
    PubMedGoogle Scholar
  • 16 Arrieta MC, Stiemsma LT, Amenyogbe N, Brown EM, Finlay B. The intestinal microbiome in early life: health and disease. Front Immunol 2014; 5: 427
    PubMedGoogle Scholar
  • 17 Holt PG. Environmental factors and primary T-cell sensitisation to inhalant allergens in infancy: reappraisal of the role of infections and air pollution. Pediatr Allergy Immunol 1995; 6 (1) 1-10
    CrossrefPubMedGoogle Scholar
  • 18 Smith PM, Garrett WS. The gut microbiota and mucosal T cells. Front Microbiol 2011; 2: 111
    PubMedGoogle Scholar
  • 19 Atarashi K, Umesaki Y, Honda K. Microbiotal influence on T cell subset development. Semin Immunol 2011; 23 (2) 146-153
    CrossrefPubMedGoogle Scholar
  • 20 Arpaia N, Campbell C, Fan X , et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013; 504 (7480) 451-455
    CrossrefPubMedGoogle Scholar
  • 21 Furusawa Y, Obata Y, Fukuda S , et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013; 504 (7480) 446-450
    CrossrefPubMedGoogle Scholar
  • 22 Romagnani S. Regulatory T cells: which role in the pathogenesis and treatment of allergic disorders?. Allergy 2006; 61 (1) 3-14
    CrossrefPubMedGoogle Scholar
  • 23 Nowak D, Suppli Ulrik C, von Mutius E. Asthma and atopy: has peak prevalence been reached?. Eur Respir J 2004; 23 (3) 359-360
    CrossrefPubMedGoogle Scholar
  • 24 The International Study of Asthma and Allergies in Childhood (ISAAC) Steering Committee. Worldwide variation in prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and atopic eczema: ISAAC. Lancet 1998; 351 (9111) 1225-1232
    CrossrefPubMedGoogle Scholar
  • 25 Strachan DP. Hay fever, hygiene, and household size. BMJ 1989; 299 (6710) 1259-1260
    CrossrefPubMedGoogle Scholar
  • 26 Romagnani S. Coming back to a missing immune deviation as the main explanatory mechanism for the hygiene hypothesis. J Allergy Clin Immunol 2007; 119 (6) 1511-1513
    CrossrefPubMedGoogle Scholar
  • 27 Yazdanbakhsh M, Kremsner PG, van Ree R. Allergy, parasites, and the hygiene hypothesis. Science 2002; 296 (5567) 490-494
    CrossrefPubMedGoogle Scholar
  • 28 Rautava S, Ruuskanen O, Ouwehand A, Salminen S, Isolauri E. The hygiene hypothesis of atopic disease—an extended version. J Pediatr Gastroenterol Nutr 2004; 38 (4) 378-388
    CrossrefPubMedGoogle Scholar
  • 29 Romagnani S. The increased prevalence of allergy and the hygiene hypothesis: missing immune deviation, reduced immune suppression, or both?. Immunology 2004; 112 (3) 352-363
    CrossrefPubMedGoogle Scholar
  • 30 Björkstén B, Naaber P, Sepp E, Mikelsaar M. The intestinal microflora in allergic Estonian and Swedish 2-year-old children. Clin Exp Allergy 1999; 29 (3) 342-346
    CrossrefPubMedGoogle Scholar
  • 31 Penders J, Thijs C, van den Brandt PA , et al. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study. Gut 2007; 56 (5) 661-667
    CrossrefPubMedGoogle Scholar
  • 32 Biasucci G, Benenati B, Morelli L, Bessi E, Boehm G. Cesarean delivery may affect the early biodiversity of intestinal bacteria. J Nutr 2008; 138 (9) 1796S-1800S
    PubMedGoogle Scholar
  • 33 Biasucci G, Rubini M, Riboni S, Morelli L, Bessi E, Retetangos C. Mode of delivery affects the bacterial community in the newborn gut. Early Hum Dev 2010; 86 (Suppl. 01) 13-15
    PubMedGoogle Scholar
  • 34 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 (4) 629-633
    CrossrefPubMedGoogle Scholar
  • 35 Martín R, Langa S, Reviriego C , et al. Human milk is a source of lactic acid bacteria for the infant gut. J Pediatr 2003; 143 (6) 754-758
    CrossrefPubMedGoogle Scholar
  • 36 Martín R, Jiménez E, Heilig H , et al. Isolation of bifidobacteria from breast milk and assessment of the bifidobacterial population by PCR-denaturing gradient gel electrophoresis and quantitative real-time PCR. Appl Environ Microbiol 2009; 75 (4) 965-969
    CrossrefPubMedGoogle Scholar
  • 37 Albesharat R, Ehrmann MA, Korakli M, Yazaji S, Vogel RF. Phenotypic and genotypic analyses of lactic acid bacteria in local fermented food, breast milk and faeces of mothers and their babies. Syst Appl Microbiol 2011; 34 (2) 148-155
    CrossrefPubMedGoogle Scholar
  • 38 Perez PF, Doré J, Leclerc M , et al. Bacterial imprinting of the neonatal immune system: lessons from maternal cells?. Pediatrics 2007; 119 (3) e724-e732
    CrossrefPubMedGoogle Scholar
  • 39 Shen Q, Tuohy KM, Gibson GR, Ward RE. In vitro measurement of the impact of human milk oligosaccharides on the faecal microbiota of weaned formula-fed infants compared to a mixture of prebiotic fructooligosaccharides and galactooligosaccharides. Lett Appl Microbiol 2011; 52 (4) 337-343
    CrossrefPubMedGoogle Scholar
  • 40 Coppa GV, Bruni S, Morelli L, Soldi S, Gabrielli O. The first prebiotics in humans: human milk oligosaccharides. J Clin Gastroenterol 2004; 38 (6, Suppl): S80-S83
    CrossrefPubMedGoogle Scholar
  • 41 Penders J, Thijs C, Vink C , et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 2006; 118 (2) 511-521
    CrossrefPubMedGoogle Scholar
  • 42 Kull I, Melen E, Alm J , et al. Breast-feeding in relation to asthma, lung function, and sensitization in young schoolchildren. J Allergy Clin Immunol 2010; 125 (5) 1013-1019
    CrossrefPubMedGoogle Scholar
  • 43 Pohlabeln H, Mühlenbruch K, Jacobs S, Böhmann H. Frequency of allergic diseases in 2-year-old children in relationship to parental history of allergy and breastfeeding. J Investig Allergol Clin Immunol 2010; 20 (3) 195-200
    PubMedGoogle Scholar
  • 44 Wright AL, Holberg CJ, Taussig LM, Martinez F. Maternal asthma status alters relation of infant feeding to asthma in childhood. Adv Exp Med Biol 2000; 478: 131-137
    PubMedGoogle Scholar
  • 45 Noverr MC, Noggle RM, Toews GB, Huffnagle GB. Role of antibiotics and fungal microbiota in driving pulmonary allergic responses. Infect Immun 2004; 72 (9) 4996-5003
    CrossrefPubMedGoogle Scholar
  • 46 Tanaka S, Kobayashi T, Songjinda P , et al. Influence of antibiotic exposure in the early postnatal period on the development of intestinal microbiota. FEMS Immunol Med Microbiol 2009; 56 (1) 80-87
    CrossrefPubMedGoogle Scholar
  • 47 Fallani M, Young D, Scott J , et al; Other Members of the INFABIO Team. Intestinal microbiota of 6-week-old infants across Europe: geographic influence beyond delivery mode, breast-feeding, and antibiotics. J Pediatr Gastroenterol Nutr 2010; 51 (1) 77-84
    CrossrefPubMedGoogle Scholar
  • 48 Jernberg C, Löfmark S, Edlund C, Jansson JK. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J 2007; 1 (1) 56-66
    CrossrefPubMedGoogle Scholar
  • 49 Salminen S, Bouley C, Boutron-Ruault MC , et al. Functional food science and gastrointestinal physiology and function. Br J Nutr 1998; 80 (Suppl. 01) S147-S171
    CrossrefPubMedGoogle Scholar
  • 50 Pessi T, Sütas Y, Hurme M, Isolauri E. Interleukin-10 generation in atopic children following oral Lactobacillus rhamnosus GG. Clin Exp Allergy 2000; 30 (12) 1804-1808
    CrossrefPubMedGoogle Scholar
  • 51 Wickens K, Black PN, Stanley TV , et al; Probiotic Study Group. A differential effect of 2 probiotics in the prevention of eczema and atopy: a double-blind, randomized, placebo-controlled trial. J Allergy Clin Immunol 2008; 122 (4) 788-794
    CrossrefPubMedGoogle Scholar
  • 52 Kalliomäki M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 2001; 357 (9262) 1076-1079
    CrossrefPubMedGoogle Scholar
  • 53 Huurre A, Laitinen K, Rautava S, Korkeamäki M, Isolauri E. Impact of maternal atopy and probiotic supplementation during pregnancy on infant sensitization: a double-blind placebo-controlled study. Clin Exp Allergy 2008; 38 (8) 1342-1348
    CrossrefPubMedGoogle Scholar
  • 54 Niers L, Martín R, Rijkers G , et al. The effects of selected probiotic strains on the development of eczema (the PandA study). Allergy 2009; 64 (9) 1349-1358
    CrossrefPubMedGoogle Scholar
  • 55 Kopp MV, Hennemuth I, Heinzmann A, Urbanek R. Randomized, double-blind, placebo-controlled trial of probiotics for primary prevention: no clinical effects of Lactobacillus GG supplementation. Pediatrics 2008; 121 (4) e850-e856
    CrossrefPubMedGoogle Scholar
  • 56 Abrahamsson TR, Jakobsson T, Böttcher MF , et al. Probiotics in prevention of IgE-associated eczema: a double-blind, randomized, placebo-controlled trial. J Allergy Clin Immunol 2007; 119 (5) 1174-1180
    CrossrefPubMedGoogle Scholar
  • 57 Kalliomäki M, Salminen S, Poussa T, Isolauri E. Probiotics during the first 7 years of life: a cumulative risk reduction of eczema in a randomized, placebo-controlled trial. J Allergy Clin Immunol 2007; 119 (4) 1019-1021
    CrossrefPubMedGoogle Scholar
  • 58 Kalliomäki M, Salminen S, Poussa T, Arvilommi H, Isolauri E. Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial. Lancet 2003; 361 (9372) 1869-1871
    CrossrefPubMedGoogle Scholar
  • 59 Kuitunen M, Kukkonen K, Juntunen-Backman K , et al. Probiotics prevent IgE-associated allergy until age 5 years in cesarean-delivered children but not in the total cohort. J Allergy Clin Immunol 2009; 123 (2) 335-341
    CrossrefPubMedGoogle Scholar
  • 60 Abrahamsson TR, Jakobsson HE, Andersson AF, Björkstén B, Engstrand L, Jenmalm MC. Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol 2012; 129 (2) 434-440 , 440.e1–440.e2
    CrossrefPubMedGoogle Scholar
  • 61 Ismail IH, Oppedisano F, Joseph SJ , et al. Reduced gut microbial diversity in early life is associated with later development of eczema but not atopy in high-risk infants. Pediatr Allergy Immunol 2012; 23 (7) 674-681
    CrossrefPubMedGoogle Scholar
  • 62 Osborn DA, Sinn JK. Prebiotics in infants for prevention of allergy. Cochrane Database Syst Rev 2013; 3: CD006474
    PubMedGoogle Scholar
  • 63 Thorburn AN, Macia L, Mackay CR. Diet, metabolites, and “western-lifestyle” inflammatory diseases. Immunity 2014; 40 (6) 833-842
    CrossrefPubMedGoogle Scholar
  • 64 Willemsen LE, Koetsier MA, van Deventer SJ, van Tol EA. Short chain fatty acids stimulate epithelial mucin 2 expression through differential effects on prostaglandin E(1) and E(2) production by intestinal myofibroblasts. Gut 2003; 52 (10) 1442-1447
    CrossrefPubMedGoogle Scholar
  • 65 Ishikawa T, Nanjo F. Dietary cycloinulooligosaccharides enhance intestinal immunoglobulin A production in mice. Biosci Biotechnol Biochem 2009; 73 (3) 677-682
    CrossrefPubMedGoogle Scholar
  • 66 Atarashi K, Tanoue T, Shima T , et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011; 331 (6015) 337-341
    CrossrefPubMedGoogle Scholar
  • 67 Atarashi K, Tanoue T, Oshima K , et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 2013; 500 (7461) 232-236
    CrossrefPubMedGoogle Scholar
  • 68 Geuking MB, Cahenzli J, Lawson MA , et al. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity 2011; 34 (5) 794-806
    CrossrefPubMedGoogle Scholar
  • 69 Geuking MB, McCoy KD, Macpherson AJ. Metabolites from intestinal microbes shape Treg. Cell Res 2013; 23 (12) 1339-1340
    CrossrefPubMedGoogle Scholar
  • 70 Devereux G. The increase in the prevalence of asthma and allergy: food for thought. Nat Rev Immunol 2006; 6 (11) 869-874
    CrossrefPubMedGoogle Scholar
  • 71 Maslowski KM, Mackay CR. Diet, gut microbiota and immune responses. Nat Immunol 2011; 12 (1) 5-9
    PubMedGoogle Scholar
  • 72 Arslanoglu S, Moro GE, Schmitt J, Tandoi L, Rizzardi S, Boehm G. Early dietary intervention with a mixture of prebiotic oligosaccharides reduces the incidence of allergic manifestations and infections during the first two years of life. J Nutr 2008; 138 (6) 1091-1095
    PubMedGoogle Scholar
  • 73 Grüber C, van Stuijvenberg M, Mosca F , et al; MIPS 1 Working Group. Reduced occurrence of early atopic dermatitis because of immunoactive prebiotics among low-atopy-risk infants. J Allergy Clin Immunol 2010; 126 (4) 791-797
    CrossrefPubMedGoogle Scholar
  • 74 van Hoffen E, Peeters KA, van Neerven RJ , et al. Effect of birch pollen-specific immunotherapy on birch pollen-related hazelnut allergy. J Allergy Clin Immunol 2011; 127 (1) 100-101 , 101.e1–e3
    CrossrefPubMedGoogle Scholar
  • 75 Passeron T, Lacour JP, Fontas E, Ortonne JP. Prebiotics and synbiotics: two promising approaches for the treatment of atopic dermatitis in children above 2 years. Allergy 2006; 61 (4) 431-437
    CrossrefPubMedGoogle Scholar
  • 76 Kukkonen K, Savilahti E, Haahtela T , et al. Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases: a randomized, double-blind, placebo-controlled trial. J Allergy Clin Immunol 2007; 119 (1) 192-198
    CrossrefPubMedGoogle Scholar
  • 77 Lemanske Jr RF, Jackson DJ, Gangnon RE , et al. Rhinovirus illnesses during infancy predict subsequent childhood wheezing. J Allergy Clin Immunol 2005; 116 (3) 571-577
    CrossrefPubMedGoogle Scholar
  • 78 Kusel MM, de Klerk NH, Kebadze T , et al. Early-life respiratory viral infections, atopic sensitization, and risk of subsequent development of persistent asthma. J Allergy Clin Immunol 2007; 119 (5) 1105-1110
    CrossrefPubMedGoogle Scholar
  • 79 Jackson DJ, Gangnon RE, Evans MD , et al. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am J Respir Crit Care Med 2008; 178 (7) 667-672
    CrossrefPubMedGoogle Scholar
  • 80 Trompette A, Gollwitzer ES, Yadava K , et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 2014; 20 (2) 159-166
    CrossrefPubMedGoogle Scholar
  • 81 Arvaniti F, Priftis KN, Papadimitriou A , et al. Adherence to the Mediterranean type of diet is associated with lower prevalence of asthma symptoms, among 10-12 years old children: the PANACEA study. Pediatr Allergy Immunol 2011; 22 (3) 283-289
    CrossrefPubMedGoogle Scholar
  • 82 Chatzi L, Kogevinas M. Prenatal and childhood Mediterranean diet and the development of asthma and allergies in children. Public Health Nutr 2009; 12 (9A): 1629-1634
    CrossrefPubMedGoogle Scholar
  • 83 Saadeh D, Salameh P, Baldi I, Raherison C. Diet and allergic diseases among population aged 0 to 18 years: myth or reality?. Nutrients 2013; 5 (9) 3399-3423
    CrossrefPubMedGoogle Scholar
  • 84 Chatzi L, Torrent M, Romieu I , et al. Mediterranean diet in pregnancy is protective for wheeze and atopy in childhood. Thorax 2008; 63 (6) 507-513
    CrossrefPubMedGoogle Scholar
  • 85 Carey OJ, Cookson JB, Britton J, Tattersfield AE. The effect of lifestyle on wheeze, atopy, and bronchial hyperreactivity in Asian and white children. Am J Respir Crit Care Med 1996; 154 (2, Pt 1) 537-540
    CrossrefPubMedGoogle Scholar
  • 86 Huang SL, Lin KC, Pan WH. Dietary factors associated with physician-diagnosed asthma and allergic rhinitis in teenagers: analyses of the first Nutrition and Health Survey in Taiwan. Clin Exp Allergy 2001; 31 (2) 259-264
    CrossrefPubMedGoogle Scholar
  • 87 Miyake Y, Sasaki S, Tanaka K, Hirota Y. Dairy food, calcium and vitamin D intake in pregnancy, and wheeze and eczema in infants. Eur Respir J 2010; 35 (6) 1228-1234
    CrossrefPubMedGoogle Scholar