Microbiota in allergy and asthma and the emerging relationship with the gut microbiome

Cell Host and Microbe

Volumn 17, Issue 5, 2015, Pages 592-602

  Fujimura, Kei E ^a   Lynch, Susan V ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; AIRWAY MICROBIOME; ALLERGENICITY; ALLERGIC ASTHMA; ALLERGIC DISEASE; ALLERGY; ASTHMA; CHILDHOOD; CLINICAL FEATURE; ENVIRONMENTAL FACTOR; HUMAN; IMMUNE RESPONSE; INTESTINE FLORA; MICROBIAL COLONIZATION; MICROBIAL COMMUNITY; MICROBIAL IMMUNITY; MICROBIOME; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; REVIEW; ANIMAL; COMPLICATION; DYSBIOSIS; GASTROINTESTINAL TRACT; HYPERSENSITIVITY; IMMUNOLOGY; MICROBIOLOGY; MICROFLORA; RESPIRATORY SYSTEM;

ANIMALS; DYSBIOSIS; ENVIRONMENTAL MICROBIOLOGY; GASTROINTESTINAL TRACT; HUMANS; HYPERSENSITIVITY; MICROBIOTA; RESPIRATORY SYSTEM;

EID: 84929308764     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2015.04.007     Document Type: Review

References (104)

1. K. Aagaard, K. Riehle, J. Ma, N. Segata, T.-A. Mistretta, C. Coarfa, S. Raza, S. Rosenbaum, I. Van den Veyver, and A. Milosavljevic A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy PLoS ONE 7 2012 e36466
2. K. Aagaard, J. Ma, K.M. Antony, R. Ganu, J. Petrosino, and J. Versalovic The placenta harbors a unique microbiome Sci. Transl. Med. 6 2014 37ra65
3. S. Accordini, A.G. Corsico, M. Braggion, M.W. Gerbase, D. Gislason, A. Gulsvik, J. Heinrich, C. Janson, D. Jarvis, and R. Jõgi The cost of persistent asthma in Europe: an international population-based study in adults Int. Arch. Allergy Immunol. 160 2013 93 101
4. I.M. Adcock, G. Caramori, and K.F. Chung New targets for drug development in asthma Lancet 372 2008 1073 1087
5. O. Akbari, P. Stock, E. Meyer, M. Kronenberg, S. Sidobre, T. Nakayama, M. Taniguchi, M.J. Grusby, R.H. DeKruyff, and D.T. Umetsu Essential role of NKT cells producing IL-4 and IL-13 in the development of allergen-induced airway hyperreactivity Nat. Med. 9 2003 582 588
6. L.J. Akinbami, J.E. Moorman, P.L. Garbe, and E.J. Sondik Status of childhood asthma in the United States, 1980-2007 Pediatrics 123 3 2009 S131 S145
7. K. Atarashi, T. Tanoue, T. Shima, A. Imaoka, T. Kuwahara, Y. Momose, G. Cheng, S. Yamasaki, T. Saito, and Y. Ohba Induction of colonic regulatory T cells by indigenous Clostridium species Science 331 2011 337 341
8. S.E. Balmer, and B.A. Wharton Diet and faecal flora in the newborn: breast milk and infant formula Arch. Dis. Child. 64 1989 1672 1677
9. M.J. Barnes, and F. Powrie Regulatory T cells reinforce intestinal homeostasis Immunity 31 2009 401 411
10. S.B.L. Barnett, and T.A. Nurmagambetov Costs of asthma in the United States: 2002-2007 J. Allergy Clin. Immunol. 127 2011 145 152
11. H. Bisgaard, M.N. Hermansen, F. Buchvald, L. Loland, L.B. Halkjaer, K. Bønnelykke, M. Brasholt, A. Heltberg, N.H. Vissing, and S.V. Thorsen Childhood asthma after bacterial colonization of the airway in neonates N. Engl. J. Med. 357 2007 1487 1495
12. H. Bisgaard, M.N. Hermansen, K. Bønnelykke, J. Stokholm, F. Baty, N.L. Skytt, J. Aniscenko, T. Kebadze, and S.L. Johnston Association of bacteria and viruses with wheezy episodes in young children: prospective birth cohort study BMJ 341 2010 c4978
13. P. Brodin, V. Jojic, T. Gao, S. Bhattacharya, C.J.L. Angel, D. Furman, S. Shen-Orr, C.L. Dekker, G.E. Swan, and A.J. Butte Variation in the human immune system is largely driven by non-heritable influences Cell 160 2015 37 47
14. C.L. Bullen, P.V. Tearle, and A.T. Willis Bifidobacteria in the intestinal tract of infants: an in-vivo study J. Med. Microbiol. 9 1976 325 333
15. R.K. Bush, and J.M. Portnoy The role and abatement of fungal allergens in allergic diseases J. Allergy Clin. Immunol. 107 2001 S430 S440
16. J. Cahenzli, Y. Köller, M. Wyss, M.B. Geuking, and K.D. McCoy Intestinal microbial diversity during early-life colonization shapes long-term IgE levels Cell Host Microbe 14 2013 559 570
17. R.N. Carmody, G.K. Gerber, J.M. Luevano Jr., D.M. Gatti, L. Somes, K.L. Svenson, and P.J. Turnbaugh Diet dominates host genotype in shaping the murine gut microbiota Cell Host Microbe 17 2015 72 84
18. E.S. Charlson, K. Bittinger, A.R. Haas, A.S. Fitzgerald, I. Frank, A. Yadav, F.D. Bushman, and R.G. Collman Topographical continuity of bacterial populations in the healthy human respiratory tract Am. J. Respir. Crit. Care Med. 184 2011 957 963
19. C.A. Cherrington, M. Hinton, G.R. Pearson, and I. Chopra Short-chain organic acids at ph 5.0 kill Escherichia coli and Salmonella spp. without causing membrane perturbation J. Appl. Bacteriol. 70 1991 161 165
20. K.F. Chung, S.E. Wenzel, J.L. Brozek, A. Bush, M. Castro, P.J. Sterk, I.M. Adcock, E.D. Bateman, E.H. Bel, and E.R. Bleecker International ERS/ATS guidelines on definition, evaluation and treatment of severe asthma Eur. Respir. J. 43 2014 343 373
21. M.J. Claesson, O. O'Sullivan, Q. Wang, J. Nikkilä, J.R. Marchesi, H. Smidt, W.M. de Vos, R.P. Ross, and P.W. O'Toole Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine PLoS ONE 4 2009 e6669
22. M.L. Conrad, R. Ferstl, R. Teich, S. Brand, N. Blümer, A.O. Yildirim, C.C. Patrascan, A. Hanuszkiewicz, S. Akira, and H. Wagner Maternal TLR signaling is required for prenatal asthma protection by the nonpathogenic microbe Acinetobacter lwoffii F78 J. Exp. Med. 206 2009 2869 2877
23. W.O.C.M. Cookson, and M.F. Moffatt Asthma: an epidemic in the absence of infection? Science 275 1997 41 42
24. E.F. Crain, K.B. Weiss, P.E. Bijur, M. Hersh, L. Westbrook, and R.E. Stein An estimate of the prevalence of asthma and wheezing among inner-city children Pediatrics 94 1994 356 362
25. T. Darville, and T. Yamauchi Respiratory syncytial virus Pediatr. Rev. 19 1998 55 61
26. J. Debarry, H. Garn, A. Hanuszkiewicz, N. Dickgreber, N. Blümer, E. von Mutius, A. Bufe, S. Gatermann, H. Renz, O. Holst, and H. Heine Acinetobacter lwoffii and Lactococcus lactis strains isolated from farm cowsheds possess strong allergy-protective properties J. Allergy Clin. Immunol. 119 2007 1514 1521
27. L. Dethlefsen, and D.A. Relman Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation Proc. Natl. Acad. Sci. USA 108 1 2011 4554 4561
28. D.B. DiGiulio, R. Romero, H.P. Amogan, J.P. Kusanovic, E.M. Bik, F. Gotsch, C.J. Kim, O. Erez, S. Edwin, and D.A. Relman Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation PLoS ONE 3 2008 e3056
29. M.G. Dominguez-Bello, E.K. Costello, M. Contreras, M. Magris, G. Hidalgo, N. Fierer, and R. Knight Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns Proc. Natl. Acad. Sci. USA 107 2010 11971 11975
30. H.J. Flint, E.A. Bayer, M.T. Rincon, R. Lamed, and B.A. White Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis Nat. Rev. Microbiol. 6 2008 121 131
31. G.E. Fox, L.J. Magrum, W.E. Balch, R.S. Wolfe, and C.R. Woese Classification of methanogenic bacteria by 16S ribosomal RNA characterization Proc. Natl. Acad. Sci. USA 74 1977 4537 4541
32. D.N. Frank, A.L. St Amand, R.A. Feldman, E.C. Boedeker, N. Harpaz, and N.R. Pace Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases Proc. Natl. Acad. Sci. USA 104 2007 13780 13785
33. N.J. Friedman, and R.S. Zeiger The role of breast-feeding in the development of allergies and asthma J. Allergy Clin. Immunol. 115 2005 1238 1248
34. K.E. Fujimura, C.C. Johnson, D.R. Ownby, M.J. Cox, E.L. Brodie, S.L. Havstad, E.M. Zoratti, K.J. Woodcroft, K.R. Bobbitt, and G. Wegienka Man's best friend? The effect of pet ownership on house dust microbial communities J. Allergy Clin. Immunol. 126 2010 410 412, e1-e3
35. K.E. Fujimura, T. Demoor, M. Rauch, A.A. Faruqi, S. Jang, C.C. Johnson, H.A. Boushey, E. Zoratti, D. Ownby, N.W. Lukacs, and S.V. Lynch House dust exposure mediates gut microbiome Lactobacillus enrichment and airway immune defense against allergens and virus infection Proc. Natl. Acad. Sci. USA 111 2014 805 810
36. Y. Furusawa, Y. Obata, S. Fukuda, T.A. Endo, G. Nakato, D. Takahashi, Y. Nakanishi, C. Uetake, K. Kato, and T. Kato Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells Nature 504 2013 446 450
37. J.E. Gereda, D.Y. Leung, A. Thatayatikom, J.E. Streib, M.R. Price, M.D. Klinnert, and A.H. Liu Relation between house-dust endotoxin exposure, type 1 T-cell development, and allergen sensitisation in infants at high risk of asthma Lancet 355 2000 1680 1683
38. M.B. Geuking, J. Cahenzli, M.A. Lawson, D.C. Ng, E. Slack, S. Hapfelmeier, K.D. McCoy, and A.J. Macpherson Intestinal bacterial colonization induces mutualistic regulatory T cell responses Immunity 34 2011 794 806
39. E. Goleva, L.P. Jackson, J.K. Harris, C.E. Robertson, E.R. Sutherland, C.F. Hall, J.T. Good Jr., E.W. Gelfand, R.J. Martin, and D.Y.M. Leung The effects of airway microbiome on corticosteroid responsiveness in asthma Am. J. Respir. Crit. Care Med. 188 2013 1193 1201
40. E.S. Gollwitzer, S. Saglani, A. Trompette, K. Yadava, R. Sherburn, K.D. McCoy, L.P. Nicod, C.M. Lloyd, and B.J. Marsland Lung microbiota promotes tolerance to allergens in neonates via PD-L1 Nat. Med. 20 2014 642 647
41. S. Gravesen Fungi as a cause of allergic disease Allergy 34 1979 135 154
42. C.G. Grulee, and H.N. Sanford The influence of breast and artificial feeding oninfantile eczema J. Pediatr. 9 1936 223 225
43. H.J. Harmsen, A.C. Wildeboer-Veloo, G.C. Raangs, A.A. Wagendorp, N. Klijn, J.G. Bindels, and G.W. Welling Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods J. Pediatr. Gastroenterol. Nutr. 30 2000 61 67
44. S. Havstad, C.C. Johnson, H. Kim, A.M. Levin, E.M. Zoratti, C.L.M. Joseph, D.R. Ownby, and G. Wegienka Atopic phenotypes identified with latent class analyses at age 2 years J. Allergy Clin. Immunol. 134 2014 722 727, e2
45. T. Herbst, A. Sichelstiel, C. Schär, K. Yadava, K. Bürki, J. Cahenzli, K. McCoy, B.J. Marsland, and N.L. Harris Dysregulation of allergic airway inflammation in the absence of microbial colonization Am. J. Respir. Crit. Care Med. 184 2011 198 205
46. B. Hesselmar, N. Åberg, B. Åberg, B. Eriksson, and B. Björkstén Does early exposure to cat or dog protect against later allergy development? Clin. Exp. Allergy 29 1999 611 617
47. M. Hilty, C. Burke, H. Pedro, P. Cardenas, A. Bush, C. Bossley, J. Davies, A. Ervine, L. Poulter, and L. Pachter Disordered microbial communities in asthmatic airways PLoS ONE 5 2010 e8578
48. Y.J. Huang, C.E. Nelson, E.L. Brodie, T.Z. Desantis, M.S. Baek, J. Liu, T. Woyke, M. Allgaier, J. Bristow, J.P. Wiener-Kronish National Heart, Lung, and Blood Institute's Asthma Clinical Research Network Airway microbiota and bronchial hyperresponsiveness in patients with suboptimally controlled asthma J. Allergy Clin. Immunol. 127 2011 372 381, e1-e3
49. C. Huttenhower, D. Gevers, R. Knight, S. Abubucker, J.H. Badger, A.T. Chinwalla, H.H. Creasy, A.M. Earl, M.G. FitzGerald, R.S. Fulton Human Microbiome Project Consortium Structure, function and diversity of the healthy human microbiome Nature 486 2012 207 214
50. I.I. Ivanov, K. Atarashi, N. Manel, E.L. Brodie, T. Shima, U. Karaoz, D. Wei, K.C. Goldfarb, C.A. Santee, and S.V. Lynch Induction of intestinal Th17 cells by segmented filamentous bacteria Cell 139 2009 485 498
51. D.J. Jackson, T.V. Hartert, F.D. Martinez, S.T. Weiss, and J.V. Fahy Asthma: NHLBI Workshop on the Primary Prevention of Chronic Lung Diseases Ann. Am. Thorac. Soc. 11 2014 S139 S145
52. C.C. Johnson, D.R. Ownby, S.H. Alford, S.L. Havstad, L.K. Williams, E.M. Zoratti, E.L. Peterson, and C.L. Joseph Antibiotic exposure in early infancy and risk for childhood atopy J. Allergy Clin. Immunol. 115 2005 1218 1224
53. S.Z. Josefowicz, R.E. Niec, H.Y. Kim, P. Treuting, T. Chinen, Y. Zheng, D.T. Umetsu, and A.Y. Rudensky Extrathymically generated regulatory T cells control mucosal TH2 inflammation Nature 482 2012 395 399
54. M. Kalliomäki, P. Kirjavainen, E. Eerola, P. Kero, S. Salminen, and E. Isolauri Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing J. Allergy Clin. Immunol. 107 2001 129 134
55. T. Kaneko, H. Mori, M. Iwata, and S. Meguro Growth stimulator for bifidobacteria produced by Propionibacterium freudenreichii and several intestinal bacteria J. Dairy Sci. 77 1994 393 404
56. A.B. Kay Allergy and allergic diseases. First of two parts N. Engl. J. Med. 344 2001 30 37
57. N.E. Klepeis, W.C. Nelson, W.R. Ott, J.P. Robinson, A.M. Tsang, P. Switzer, J.V. Behar, S.C. Hern, and W.H. Engelmann The National Human Activity Pattern Survey (NHAPS): a resource for assessing exposure to environmental pollutants J. Expo. Anal. Environ. Epidemiol. 11 2001 231 252
58. K.M. Kloepfer, W.M. Lee, T.E. Pappas, T.J. Kang, R.F. Vrtis, M.D. Evans, R.E. Gangnon, Y.A. Bochkov, D.J. Jackson, R.F. Lemanske Jr., and J.E. Gern Detection of pathogenic bacteria during rhinovirus infection is associated with increased respiratory symptoms and asthma exacerbations J. Allergy Clin. Immunol. 133 2014 1301 1307, e1-e3
59. M. Kraft The role of bacterial infections in asthma Clin. Chest Med. 21 2000 301 313
60. I. Kull, E. Melen, J. Alm, J. Hallberg, M. Svartengren, M. van Hage, G. Pershagen, M. Wickman, and A. Bergström Breast-feeding in relation to asthma, lung function, and sensitization in young schoolchildren J. Allergy Clin. Immunol. 125 2010 1013 1019
61. V.P. Kurup, H.-D. Shen, and B. Banerjee Respiratory fungal allergy Microbes Infect. 2 2000 1101 1110
62. S. Lee, J. Sung, J. Lee, and G. Ko Comparison of the gut microbiotas of healthy adult twins living in South Korea and the United States Appl. Environ. Microbiol. 77 2011 7433 7437
63. K.P. Lemon, V. Klepac-Ceraj, H.K. Schiffer, E.L. Brodie, S.V. Lynch, and R. Kolter Comparative analyses of the bacterial microbiota of the human nostril and oropharynx MBio 1 2010 4 6
64. S.V. Lynch, R.A. Wood, H. Boushey, L.B. Bacharier, G.R. Bloomberg, M. Kattan, G.T. O'Connor, M.T. Sandel, A. Calatroni, and E. Matsui Effects of early-life exposure to allergens and bacteria on recurrent wheeze and atopy in urban children J. Allergy Clin. Immunol. 134 2014 593 601, e12
65. P.R. Marri, D.A. Stern, A.L. Wright, D. Billheimer, and F.D. Martinez Asthma-associated differences in microbial composition of induced sputum J. Allergy Clin. Immunol. 131 2013 346 352.e1-3
66. K.M. Maslowski, A.T. Vieira, A. Ng, J. Kranich, F. Sierro, D. Yu, H.C. Schilter, M.S. Rolph, F. Mackay, and D. Artis Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43 Nature 461 2009 1282 1286
67. M. Masoli, D. Fabian, S. Holt, R. Beasley Global Initiative for Asthma (GINA) Program The global burden of asthma: executive summary of the GINA Dissemination Committee report Allergy 59 2004 469 478
68. S.K. Mazmanian, J.L. Round, and D.L. Kasper A microbial symbiosis factor prevents intestinal inflammatory disease Nature 453 2008 620 625
69. C. Nembrini, A. Sichelstiel, J. Kisielow, M. Kurrer, M. Kopf, and B.J. Marsland Bacterial-induced protection against allergic inflammation through a multicomponent immunoregulatory mechanism Thorax 66 2011 755 763
70. C. Ober, and T.-C. Yao The genetics of asthma and allergic disease: a 21st century perspective Immunol. Rev. 242 2011 10 30
71. J. Ochoa-Repáraz, D.W. Mielcarz, L.E. Ditrio, A.R. Burroughs, S. Begum-Haque, S. Dasgupta, D.L. Kasper, and L.H. Kasper Central nervous system demyelinating disease protection by the human commensal Bacteroides fragilis depends on polysaccharide A expression J. Immunol. 185 2010 4101 4108
72. T. Olszak, D. An, S. Zeissig, M.P. Vera, J. Richter, A. Franke, J.N. Glickman, R. Siebert, R.M. Baron, D.L. Kasper, and R.S. Blumberg Microbial exposure during early life has persistent effects on natural killer T cell function Science 336 2012 489 493
73. D.R. Ownby, C.C. Johnson, and E.L. Peterson Exposure to dogs and cats in the first year of life and risk of allergic sensitization at 6 to 7 years of age JAMA 288 2002 963 972
74. J. Penders, E.E. Stobberingh, C. Thijs, H. Adams, C. Vink, R. van Ree, and P.A. van den Brandt Molecular fingerprinting of the intestinal microbiota of infants in whom atopic eczema was or was not developing Clin. Exp. Allergy 36 2006 1602 1608
75. J. Penders, E.E. Stobberingh, P.A. van den Brandt, and C. Thijs The role of the intestinal microbiota in the development of atopic disorders Allergy 62 2007 1223 1236
76. J.R. Porter Antony van Leeuwenhoek: tercentenary of his discovery of bacteria Bacteriol. Rev. 40 1976 260 269
77. J. Qin, R. Li, J. Raes, M. Arumugam, K.S. Burgdorf, C. Manichanh, T. Nielsen, N. Pons, F. Levenez, T. Yamada MetaHIT Consortium A human gut microbial gene catalogue established by metagenomic sequencing Nature 464 2010 59 65
78. D. Rastogi, S.M. Canfield, A. Andrade, C.R. Isasi, C.B. Hall, A. Rubinstein, and R. Arens Obesity-associated asthma in children: a distinct entity Chest 141 2012 895 905
79. H. Renz-Polster, M.R. David, A.S. Buist, W.M. Vollmer, E.A. O'Connor, E.A. Frazier, and M.A. Wall Caesarean section delivery and the risk of allergic disorders in childhood Clin. Exp. Allergy 35 2005 1466 1472
80. W.E.W. Roediger Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man Gut 21 1980 793 798
81. G.A. Rook 99th Dahlem conference on infection, inflammation and chronic inflammatory disorders: darwinian medicine and the "hygiene" or "old friends" hypothesis Clin. Exp. Immunol. 160 2010 70 79
82. J.L. Round, and S.K. Mazmanian Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota Proc. Natl. Acad. Sci. USA 107 2010 12204 12209
83. Y.P. Rubtsov, J.P. Rasmussen, E.Y. Chi, J. Fontenot, L. Castelli, X. Ye, P. Treuting, L. Siewe, A. Roers, and W.R. Henderson Jr. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces Immunity 28 2008 546 558
84. D.C. Savage Microbial ecology of the gastrointestinal tract Annu. Rev. Microbiol. 31 1977 107 133
85. A. Simpson, V.Y.F. Tan, J. Winn, M. Svensén, C.M. Bishop, D.E. Heckerman, I. Buchan, and A. Custovic Beyond atopy: multiple patterns of sensitization in relation to asthma in a birth cohort study Am. J. Respir. Crit. Care Med. 181 2010 1200 1206
86. K. Smith, K.D. McCoy, and A.J. Macpherson Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota Semin. Immunol. 19 2007 59 69
87. P.M. Smith, M.R. Howitt, N. Panikov, M. Michaud, C.A. Gallini, M. Bohlooly-Y, J.N. Glickman, and W.S. Garrett The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis Science 341 2013 569 573
88. H. Sokol, B. Pigneur, L. Watterlot, O. Lakhdari, L.G. Bermúdez-Humarán, J.J. Gratadoux, S. Blugeon, C. Bridonneau, J.P. Furet, and G. Corthier Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients Proc. Natl. Acad. Sci. USA 105 2008 16731 16736
89. R.T. Stein, D. Sherrill, W.J. Morgan, C.J. Holberg, M. Halonen, L.M. Taussig, A.L. Wright, and F.D. Martinez Respiratory syncytial virus in early life and risk of wheeze and allergy by age 13 years Lancet 354 1999 541 545
90. L.G. Stensballe, J. Simonsen, S.M. Jensen, K. Bønnelykke, and H. Bisgaard Use of antibiotics during pregnancy increases the risk of asthma in early childhood J. Pediatr. 162 2013 832 838, e3
91. D.P. Strachan Hay fever, hygiene, and household size BMJ 299 1989 1259 1260
92. S.M. Teo, D. Mok, K. Pham, M. Kusel, M. Serralha, N. Troy, B.J. Holt, B.J. Hales, M.L. Walker, and E. Hollams The Infant Nasopharyngeal Microbiome Impacts Severity of Lower Respiratory Infection and Risk of Asthma Development Cell Host Microbe 17 2015 1 12
93. Y. Tomosada, E. Chiba, H. Zelaya, T. Takahashi, K. Tsukida, H. Kitazawa, S. Alvarez, and J. Villena Nasally administered Lactobacillus rhamnosus strains differentially modulate respiratory antiviral immune responses and induce protection against respiratory syncytial virus infection BMC Immunol. 14 2013 40
94. A. Trompette, E.S. Gollwitzer, K. Yadava, A.K. Sichelstiel, N. Sprenger, C. Ngom-Bru, C. Blanchard, T. Junt, L.P. Nicod, N.L. Harris, and B.J. Marsland Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis Nat. Med. 20 2014 159 166
95. M. Tsoumakidou, W. Elston, J. Zhu, Z. Wang, E. Gamble, N.M. Siafakas, N.C. Barnes, and P.K. Jeffery Cigarette smoking alters bronchial mucosal immunity in asthma Am. J. Respir. Crit. Care Med. 175 2007 919 925
96. P.J. Turnbaugh, M. Hamady, T. Yatsunenko, B.L. Cantarel, A. Duncan, R.E. Ley, M.L. Sogin, W.J. Jones, B.A. Roe, and J.P. Affourtit A core gut microbiome in obese and lean twins Nature 457 2009 480 484
97. M. Vissers, R. de Groot, and G. Ferwerda Severe viral respiratory infections: are bugs bugging? Mucosal Immunol. 7 2014 227 238
98. M.J. Wannemuehler, A.M. Overstreet, D.V. Ward, and G.J. Phillips Draft genome sequences of the altered schaedler flora, a defined bacterial community from gnotobiotic mice Genome Announc 2 2014 e00287-e14
99. K.B. Weiss, P.J. Gergen, and E.F. Crain Inner-city asthma. The epidemiology of an emerging US public health concern Chest 101 1992 362S 367S
100. S. Winker, and C.R. Woese A definition of the domains Archaea, Bacteria and Eucarya in terms of small subunit ribosomal RNA characteristics Syst. Appl. Microbiol. 14 1991 305 310
101. C.R. Woese Bacterial Evolution Background Microbiology 51 1987 221 271
102. P.G. Woodruff, B. Modrek, D.F. Choy, G. Jia, A.R. Abbas, A. Ellwanger, L.L. Koth, J.R. Arron, and J.V. Fahy T-helper type 2-driven inflammation defines major subphenotypes of asthma Am. J. Respir. Crit. Care Med. 180 2009 388 395
103. T. Yatsunenko, F.E. Rey, M.J. Manary, I. Trehan, M.G. Dominguez-Bello, M. Contreras, M. Magris, G. Hidalgo, R.N. Baldassano, and A.P. Anokhin Human gut microbiome viewed across age and geography Nature 486 2012 222 227
104. H. Yoshioka, K. Iseki, and K. Fujita Development and differences of intestinal flora in the neonatal period in breast-fed and bottle-fed infants Pediatrics 72 1983 317 321