Host–microbe interactions in distal airways: Relevance to chronic airway diseases

European Respiratory Review

Volumn 24, Issue 135, 2015, Pages 78-91

  Martin, Clémence ^a   Burgel, Pierre Régis ^a   Lepage, Patricia ^b   Andréjak, Claire ^c   De Blic, Jacques ^d   Bourdin, Arnaud ^e   Brouard, Jacques ^f   Chanez, Pascal ^g   Dalphin, Jean Charles ^h   Deslée, Gaetan ⁱ   Deschildre, Antoine ^j   Gosset, Philippe ^g,k   Touqui, Lhousseine ^l   Dusser, Daniel ^a  

^a université Paris Cité   (France)

^b UMR1319 MICALIS   (France)

^c AMIENS UNIVERSITY HOSPITAL   (France)

^d HÔPITAL NECKER ENFANTS MALADES   (France)

^e HÔPITAL ARNAUD DE VILLENEUVE   (France)

^f CAEN UNIVERSITY HOSPITAL   (France)

^g INSERM   (France)

^h UNIVERSITY HOSPITAL JEAN MINJOZ   (France)

ⁱ REIMS UNIVERSITY HOSPITAL   (France)

^j LILLE UNIVERSITY HOSPITAL   (France)

^k INSTITUT PASTEUR   (France)

^l INSERM U1019   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; ASTHMA; ATYPICAL MYCOBACTERIUM; BACTERIAL GENOME; BACTERIAL INFECTION; BRONCHIECTASIS; BRONCHIOLITIS OBLITERANS; CELLULAR IMMUNITY; CHRONIC OBSTRUCTIVE LUNG DISEASE; CHRONIC RESPIRATORY TRACT DISEASE; CYSTIC FIBROSIS; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIOME; NONHUMAN; PHAGOCYTE; REVIEW; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS INFECTION; INTESTINE FLORA; LUNG; MICROBIOLOGY; MICROFLORA; MYCOBACTERIUM; PATHOGENICITY; PATHOPHYSIOLOGY; RESPIRATORY TRACT DISEASE; VIROLOGY;

ASTHMA; BRONCHIECTASIS; CYSTIC FIBROSIS; GASTROINTESTINAL MICROBIOME; HOST-PATHOGEN INTERACTIONS; HUMANS; LUNG; MICROBIOTA; MYCOBACTERIUM; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RESPIRATORY TRACT DISEASES;

EID: 84923861205     PISSN: 09059180     EISSN: 16000617     Source Type: Journal    
DOI: 10.1183/09059180.00011614     Document Type: Review

References (161)

1. Burgel PR, de Blic J, Chanez P, et al. Update on the roles of distal airways in asthma. Eur Respir Rev 2009; 18: 80–95.
2. Burgel PR, Bourdin A, Chanez P, et al. Update on the roles of distal airways in COPD. Eur Respir Rev 2011; 20: 7–22.
3. Burgel PR, Bergeron A, de Blic J, et al. Small airways diseases, excluding asthma and COPD: an overview. Eur Respir Rev 2013; 22: 131–147.
4. Burgel PR, Montani D, Danel C, et al. A morphometric study of mucins and small airway plugging in cystic fibrosis. Thorax 2007; 62: 153–161.
5. Yanai M, Sekizawa K, Ohrui T, et al. Site of airway obstruction in pulmonary disease: direct measurement of intrabronchial pressure. J Appl Physiol (1985) 1992; 72: 1016–1023.
6. Hogg JC, Macklem PT, Thurlbeck WM. Site and nature of airway obstruction in chronic obstructive lung disease. N Engl J Med 1968; 278: 1355–1360.
7. McDonough JE, Yuan R, Suzuki M, et al. Small-airway obstruction and emphysema in chronic obstructive pulmonary disease. N Engl J Med 2011; 365: 1567–1575.
8. Verleden SE, Vasilescu DM, Willems S, et al. The site and nature of airway obstruction after lung transplantation. Am J Respir Crit Care Med 2014; 189: 292–300.
9. Mitzner W. Emphysema–a disease of small airways or lung parenchyma? N Engl J Med 2011; 365: 1637–1639.
10. Hogg JC, Chu F, Utokaparch S, et al. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med 2004; 350: 2645–2653.
11. Sethi S. Chronic obstructive pulmonary disease and infection. Disruption of the microbiome? Ann Am Thorac Soc 2014; 11; Suppl. 1, S43–S47.
12. Berenson CS, Kruzel RL, Eberhardt E, et al. Impaired innate immune alveolar macrophage response and the predilection for COPD exacerbations. Thorax 2014; 69: 811–818.
13. Relman DA. Microbiology: learning about who we are. Nature 2012; 486: 194–195.
14. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 2012; 486: 207–214.
15. Human Microbiome Project Consortium. A framework for human microbiome research. Nature 2012; 486: 215–221.
16. Huang YJ, Charlson ES, Collman RG, et al. The role of the lung microbiome in health and disease. A National Heart, Lung, and Blood Institute workshop report. Am J Respir Crit Care Med 2013; 187: 1382–1387.
17. Suau A, Bonnet R, Sutren M, et al. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microbiol 1999; 65: 4799–4807.
18. Zoetendal EG, Rajilic-Stojanovic M, de Vos WM. High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut 2008; 57: 1605–1615.
19. Mackie RI, Sghir A, Gaskins HR. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 1999; 69: 1035S–1045S.
20. De La Cochetiere MF, Durand T, Lepage P, et al. Resilience of the dominant human fecal microbiota upon short-course antibiotic challenge. J Clin Microbiol 2005; 43: 5588–5592.
21. Tap J, Mondot S, Levenez F, et al. Towards the human intestinal microbiota phylogenetic core. Environ Microbiol 2009; 11: 2574–2584.
22. Rondon MR, Raffel SJ, Goodman RM, et al. Toward functional genomics in bacteria: analysis of gene expression in Escherichia coli from a bacterial artificial chromosome library of Bacillus cereus. Proc Natl Acad Sci USA 1999; 96: 6451–6455.
23. Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010; 464: 59–65.
24. Arumugam M, Raes J, Pelletier E, et al. Enterotypes of the human gut microbiome. Nature 2011; 473: 174–180.
25. Tamboli CP, Neut C, Desreumaux P, et al. Dysbiosis as a prerequisite for IBD. Gut 2004; 53: 1057.
26. Nagalingam NA, Lynch SV. Role of the microbiota in inflammatory bowel diseases. Inflamm Bowel Dis 2012; 18: 968–984.
27. Cotillard A, Kennedy SP, Kong LC, et al. Dietary intervention impact on gut microbial gene richness. Nature 2013; 500: 585–588.
28. Han MK, Huang YJ, Lipuma JJ, et al. Significance of the microbiome in obstructive lung disease. Thorax 2012; 67: 456–463.
29. Dickson RP, Martinez FJ, Huffnagle GB. The role of the microbiome in exacerbations of chronic lung diseases. Lancet 2014; 384: 691–702.
30. O’Sullivan BP, Freedman SD. Cystic fibrosis. Lancet 2009; 373: 1891–1904.
31. UK Cystic Fibrosis Registry. Annual Data Report 2012. www.cysticfibrosis.org.uk/media/316760/Scientific%20Registry%20Review%202012.pdf Date last updated: September 2013. Date last accessed: January 22, 2015.
32. Worlitzsch D, Tarran R, Ulrich M, et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 2002; 109: 317–325.
33. Ulrich M, Herbert S, Berger J, et al. Localization of Staphylococcus aureus in infected airways of patients with cystic fibrosis and in a cell culture model of S. aureus adherence. Am J Respir Cell Mol Biol 1998; 19: 83–91.
34. Linnane BM, Hall GL, Nolan G, et al. Lung function in infants with cystic fibrosis diagnosed by newborn screening. Am J Respir Crit Care Med 2008; 178: 1238–1244.
35. Armstrong DS, Grimwood K, Carlin JB, et al. Bronchoalveolar lavage or oropharyngeal cultures to identify lower respiratory pathogens in infants with cystic fibrosis. Pediatr Pulmonol 1996; 21: 267–275.
36. Sly PD, Brennan S, Gangell C, et al. Lung disease at diagnosis in infants with cystic fibrosis detected by newborn screening. Am J Respir Crit Care Med 2009; 180: 146–152.
37. Armstrong DS, Grimwood K, Carlin JB, et al. Lower airway inflammation in infants and young children with cystic fibrosis. Am J Respir Crit Care Med 1997; 156: 1197–1204.
38. Ramsey KA, Ranganathan S, Park J, et al. Early respiratory infection is associated with reduced spirometry in children with cystic fibrosis. Am J Respir Crit Care Med 2014; 190: 1111–1116.
39. Goss CH, Mayer-Hamblett N, Aitken ML, et al. Association between Stenotrophomonas maltophilia and lung function in cystic fibrosis. Thorax 2004; 59: 955–959.
40. Dalboge CS, Hansen CR, Pressler T, et al. Chronic pulmonary infection with Stenotrophomonas maltophilia and lung function in patients with cystic fibrosis. J Cyst Fibros 2011; 10: 318–325.
41. Ronne Hansen C, Pressler T, Hoiby N, et al. Chronic infection with Achromobacter xylosoxidans in cystic fibrosis patients; a retrospective case control study. J Cyst Fibros 2006; 5: 245–251.
42. De Baets F, Schelstraete P, Van Daele S, et al. Achromobacter xylosoxidans in cystic fibrosis: prevalence and clinical relevance. J Cyst Fibros 2007; 6: 75–78.
43. Hansen CR, Pressler T, Nielsen KG, et al. Inflammation in Achromobacter xylosoxidans infected cystic fibrosis patients. J Cyst Fibros 2010; 9: 51–58.
44. Flume PA, Yankaskas JR, Ebeling M, et al. Massive hemoptysis in cystic fibrosis. Chest 2005; 128: 729–738.
45. Wolter DJ, Emerson JC, McNamara S, et al. Staphylococcus aureus small-colony variants are independently associated with worse lung disease in children with cystic fibrosis. Clin Infect Dis 2013; 57: 384–391.
46. Dasenbrook EC, Checkley W, Merlo CA, et al. Association between respiratory tract methicillin-resistant Staphylococcus aureus and survival in cystic fibrosis. JAMA 2010; 303: 2386–2392.
47. Pillarisetti N, Williamson E, Linnane B, et al. Infection, inflammation, and lung function decline in infants with cystic fibrosis. Am J Respir Crit Care Med 2011; 184: 75–81.
48. Gangell C, Gard S, Douglas T, et al. Inflammatory responses to individual microorganisms in the lungs of children with cystic fibrosis. Clin Infect Dis 2011; 53: 425–432.
49. Sly PD, Gangell CL, Chen L, et al. Risk factors for bronchiectasis in children with cystic fibrosis. N Engl J Med 2013; 368: 1963–1970.
50. Tunney MM, Field TR, Moriarty TF, et al. Detection of anaerobic bacteria in high numbers in sputum from patients with cystic fibrosis. Am J Respir Crit Care Med 2008; 177: 995–1001.
51. Blumer JL, Saiman L, Konstan MW, et al. The efficacy and safety of meropenem and tobramycin vs ceftazidime and tobramycin in the treatment of acute pulmonary exacerbations in patients with cystic fibrosis. Chest 2005; 128: 2336–2346.
52. Bittar F, Rolain JM. Detection and accurate identification of new or emerging bacteria in cystic fibrosis patients. Clin Microbiol Infect 2010; 16: 809–820.
53. Klepac-Ceraj V, Lemon KP, Martin TR, et al. Relationship between cystic fibrosis respiratory tract bacterial communities and age, genotype, antibiotics and Pseudomonas aeruginosa. Environ Microbiol 2010; 12: 1293–1303.
54. Cox MJ, Allgaier M, Taylor B, et al. Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PLoS One 2010; 5: e11044.
55. Goddard AF, Staudinger BJ, Dowd SE, et al. Direct sampling of cystic fibrosis lungs indicates that DNA-based analyses of upper-airway specimens can misrepresent lung microbiota. Proc Natl Acad Sci USA 2012; 109: 13769–13774.
56. van der Gast CJ, Walker AW, Stressmann FA, et al. Partitioning core and satellite taxa from within cystic fibrosis lung bacterial communities. ISME J 2011; 5: 780–791.
57. Guss AM, Roeselers G, Newton IL, et al. Phylogenetic and metabolic diversity of bacteria associated with cystic fibrosis. ISME J 2011; 5: 20–29.
58. Sze MA, Dimitriu PA, Hayashi S, et al. The lung tissue microbiome in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2012; 185: 1073–1080.
59. Bittar F, Richet H, Dubus JC, et al. Molecular detection of multiple emerging pathogens in sputa from cystic fibrosis patients. PLoS One 2008; 3: e2908.
60. Fodor AA, Klem ER, Gilpin DF, et al. The adult cystic fibrosis airway microbiota is stable over time and infection type, and highly resilient to antibiotic treatment of exacerbations. PLoS One 2012; 7: e45001.
61. Stressmann FA, Rogers GB, van der Gast CJ, et al. Long-term cultivation-independent microbial diversity analysis demonstrates that bacterial communities infecting the adult cystic fibrosis lung show stability and resilience. Thorax 2012; 67: 867–873.
62. Filkins LM, Hampton TH, Gifford AH, et al. Prevalence of streptococci and increased polymicrobial diversity associated with cystic fibrosis patient stability. J Bacteriol 2012; 194: 4709–4717.
63. Zhao J, Schloss PD, Kalikin LM, et al. Decade-long bacterial community dynamics in cystic fibrosis airways. Proc Natl Acad Sci USA 2012; 109: 5809–5814.
64. Stoltz DA, Meyerholz DK, Pezzulo AA, et al. Cystic fibrosis pigs develop lung disease and exhibit defective bacterial eradication at birth. Sci Transl Med 2010; 2: 29ra31.
65. Pezzulo AA, Tang XX, Hoegger MJ, et al. Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 2012; 487: 109–113.
66. Sibley CD, Duan K, Fischer C, et al. Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections. PLoS Pathog 2008; 4: e1000184.
67. Zhao J, Murray S, Lipuma JJ. Modeling the impact of antibiotic exposure on human microbiota. Sci Rep 2014; 4: 4345.
68. Dethlefsen L, Relman DA. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci USA 2011; 108: Suppl. 1, 4554–4561.
69. Clancy JP, Jain M. Personalized medicine in cystic fibrosis: dawning of a new era. Am J Respir Crit Care Med 2012; 186: 593–597.
70. Martinez-Garcia MA, de Gracia J, Vendrell Relat M, et al. Multidimensional approach to non-cystic fibrosis bronchiectasis: the FACED score. Eur Respir J 2014; 43: 1357–1367.
71. Rogers GB, van der Gast CJ, Cuthbertson L, et al. Clinical measures of disease in adult non-CF bronchiectasis correlate with airway microbiota composition. Thorax 2013; 68: 731–737.
72. Rogers GB, Zain NM, Bruce KD, et al. A novel microbiota stratification system predicts future exacerbations in bronchiectasis. Ann Am Thorac Soc 2014; 11: 496–503.
73. Rogers GB, van der Gast CJ, Serisier DJ. Predominant pathogen competition and core microbiota divergence in chronic airway infection. ISME J 2015; 9: 217–225.
74. Sethi S, Murphy TF. Infection in the pathogenesis and course of chronic obstructive pulmonary disease. N Engl J Med 2008; 359: 2355–2365.
75. Sethi S, Maloney J, Grove L, et al. Airway inflammation and bronchial bacterial colonization in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2006; 173: 991–998.
76. Weinreich UM, Korsgaard J. Bacterial colonisation of lower airways in health and chronic lung disease. Clin Respir J 2008; 2: 116–122.
77. Rosell A, Monso E, Soler N, et al. Microbiologic determinants of exacerbation in chronic obstructive pulmonary disease. Arch Intern Med 2005; 165: 891–897.
78. Bandi V, Apicella MA, Mason E, et al. Nontypeable Haemophilus influenzae in the lower respiratory tract of patients with chronic bronchitis. Am J Respir Crit Care Med 2001; 164: 2114–2119.
79. Zhang M, Li Q, Zhang XY, et al. Relevance of lower airway bacterial colonization, airway inflammation, and pulmonary function in the stable stage of chronic obstructive pulmonary disease. Eur J Clin Microbiol Infect Dis 2010; 29: 1487–1493.
80. Patel IS, Vlahos I, Wilkinson TM, et al. Bronchiectasis, exacerbation indices, and inflammation in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2004; 170: 400–407.
81. Sethi S, Evans N, Grant BJ, et al. New strains of bacteria and exacerbations of chronic obstructive pulmonary disease. N Engl J Med 2002; 347: 465–471.
82. Sethi S, Wrona C, Eschberger K, et al. Inflammatory profile of new bacterial strain exacerbations of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2008; 177: 491–497.
83. Erb-Downward JR, Thompson DL, Han MK, et al. Analysis of the lung microbiome in the “healthy” smoker and in COPD. PLoS One 2011; 6: e16384.
84. Morris A, Beck JM, Schloss PD, et al. Comparison of the respiratory microbiome in healthy nonsmokers and smokers. Am J Respir Crit Care Med 2013; 187: 1067–1075.
85. Zakharkina T, Heinzel E, Koczulla RA, et al. Analysis of the airway microbiota of healthy individuals and patients with chronic obstructive pulmonary disease by T-RFLP and clone sequencing. PLoS One 2013; 8: e68302.
86. Molyneaux PL, Mallia P, Cox MJ, et al. Outgrowth of the bacterial airway microbiome after rhinovirus exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2013; 188: 1224–1231.
87. Braun-Fahrlander C, Riedler J, Herz U, et al. Environmental exposure to endotoxin and its relation to asthma in school-age children. N Engl J Med 2002; 347: 869–877.
88. Fyhrquist N, Ruokolainen L, Suomalainen A, et al. Acinetobacter species in the skin microbiota protects against allergic sensitization and inflammation. J Allergy Clin Immunol 2014; 134: 1301–1309.
89. Trompette A, Gollwitzer ES, Yadava K, et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 2014; 20: 159–166.
90. Ege MJ, Mayer M, Normand AC, et al. Exposure to environmental microorganisms and childhood asthma. N Engl J Med 2011; 364: 701–709.
91. Maslowski KM, Mackay CR. Diet, gut microbiota and immune responses. Nat Immunol 2011; 12: 5–9.
92. Schram-Bijkerk D, Doekes G, Douwes J, et al. Bacterial and fungal agents in house dust and wheeze in children: the PARSIFAL study. Clin Exp Allergy 2005; 35: 1272–1278.
93. Herbst T, Sichelstiel A, Schar C, et al. Dysregulation of allergic airway inflammation in the absence of microbial colonization. Am J Respir Crit Care Med 2011; 184: 198–205.
94. Hilty M, Burke C, Pedro H, et al. Disordered microbial communities in asthmatic airways. PLoS One 2010; 5: e8578.
95. Huang YJ, Nelson CE, Brodie EL, et al. Airway microbiota and bronchial hyperresponsiveness in patients with suboptimally controlled asthma. J Allergy Clin Immunol 2011; 127: 372–381.
96. Marri PR, Stern DA, Wright AL, et al. Asthma-associated differences in microbial composition of induced sputum. J Allergy Clin Immunol 2013; 131: 346–352.
97. Le Bourgeois M, Goncalves M, Le Clainche L, et al. Bronchoalveolar cells in children <3 years old with severe recurrent wheezing. Chest 2002; 122: 791–797.
98. Saglani S, Nicholson AG, Scallan M, et al. Investigation of young children with severe recurrent wheeze: any clinical benefit? Eur Respir J 2006; 27: 29–35.
99. Saito J, Harris WT, Gelfond J, et al. Physiologic, bronchoscopic, and bronchoalveolar lavage fluid findings in young children with recurrent wheeze and cough. Pediatr Pulmonol 2006; 41: 709–719.
100. Schwerk N, Brinkmann F, Soudah B, et al. Wheeze in preschool age is associated with pulmonary bacterial infection and resolves after antibiotic therapy. PLoS One 2011; 6: e27913.
101. Nagayama Y, Tsubaki T, Nakayama S, et al. Bacterial colonization in respiratory secretions from acute and recurrent wheezing infants and children. Pediatr Allergy Immunol 2007; 18: 110–117.
102. Zhang Q, Illing R, Hui CK, et al. Bacteria in sputum of stable severe asthma and increased airway wall thickness. Respir Res 2012; 13: 35.
103. Bisgaard H, Hermansen MN, Buchvald F, et al. Childhood asthma after bacterial colonization of the airway in neonates. N Engl J Med 2007; 357: 1487–1495.
104. Folsgaard NV, Schjorring S, Chawes BL, et al. Pathogenic bacteria colonizing the airways in asymptomatic neonates stimulates topical inflammatory mediator release. Am J Respir Crit Care Med 2013; 187: 589–595.
105. Goleva E, Jackson LP, Harris JK, et al. The effects of airway microbiome on corticosteroid responsiveness in asthma. Am J Respir Crit Care Med 2013; 188: 1193–1201.
106. Yusen RD, Christie JD, Edwards LB, et al. The Registry of the International Society for Heart and Lung Transplantation: Thirtieth Adult Lung and Heart-Lung Transplant Report–2013; focus theme: age. J Heart Lung Transplant 2013; 32: 965–978.
107. Vos R, Vanaudenaerde BM, Geudens N, et al. Pseudomonal airway colonisation: risk factor for bronchiolitis obliterans syndrome after lung transplantation? Eur Respir J 2008; 31: 1037–1045.
108. Botha P, Archer L, Anderson RL, et al. Pseudomonas aeruginosa colonization of the allograft after lung transplantation and the risk of bronchiolitis obliterans syndrome. Transplantation 2008; 85: 771–774.
109. Dickson RP, Erb-Downward JR, Freeman CM, et al. Changes in the lung microbiome following lung transplantation include the emergence of two distinct pseudomonas species with distinct clinical associations. PLoS One 2014; 9: e97214.
110. Willner DL, Hugenholtz P, Yerkovich ST, et al. Reestablishment of recipient-associated microbiota in the lung allograft is linked to reduced risk of bronchiolitis obliterans syndrome. Am J Respir Crit Care Med 2013; 187: 640–647.
111. Kubo K, Yamazaki Y, Masubuchi T, et al. Pulmonary infection with Mycobacterium avium-intracellulare leads to air trapping distal to the small airways. Am J Respir Crit Care Med 1998; 158: 979–984.
112. Andréjak C, Nielsen R, Thomsen VO, et al. Chronic respiratory disease, inhaled corticosteroids and risk of non-tuberculous mycobacteriosis. Thorax 2013; 68: 256–262.
113. Huang CT, Tsai YJ, Wu HD, et al. Impact of non-tuberculous mycobacteria on pulmonary function decline in chronic obstructive pulmonary disease. Int J Tuberc Lung Dis 2012; 16: 539–545.
114. Hojo M, Iikura M, Hirano S, et al. Increased risk of nontuberculous mycobacterial infection in asthmatic patients using long-term inhaled corticosteroid therapy. Respirology 2012; 17: 185–190.
115. Esther CR Jr, Esserman DA, Gilligan P, et al. Chronic Mycobacterium abscessus infection and lung function decline in cystic fibrosis. J Cyst Fibros 2010; 9: 117–123.
116. Olivier KN, Weber DJ, Lee JH, et al. Nontuberculous mycobacteria. II: nested-cohort study of impact on cystic fibrosis lung disease. Am J Respir Crit Care Med 2003; 167: 835–840.
117. Embil J, Warren P, Yakrus M, et al. Pulmonary illness associated with exposure to Mycobacterium-avium complex in hot tub water. Hypersensitivity pneumonitis or infection? Chest 1997; 111: 813–816.
118. Kahana LM, Kay JM, Yakrus MA, et al. Mycobacterium avium complex infection in an immunocompetent young adult related to hot tub exposure. Chest 1997; 111: 242–245.
119. Tillie-Leblond I, Grenouillet F, Reboux G, et al. Hypersensitivity pneumonitis and metalworking fluids contaminated by mycobacteria. Eur Respir J 2011; 37: 640–647.
120. Flight WG, Bright-Thomas RJ, Tilston P, et al. Incidence and clinical impact of respiratory viruses in adults with cystic fibrosis. Thorax 2014; 69: 247–253.
121. van Ewijk BE, van der Zalm MM, Wolfs TF, et al. Prevalence and impact of respiratory viral infections in young children with cystic fibrosis: prospective cohort study. Pediatrics 2008; 122: 1171–1176.
122. Wat D, Gelder C, Hibbitts S, et al. The role of respiratory viruses in cystic fibrosis. J Cyst Fibros 2008; 7: 320–328.
123. de Almeida MB, Zerbinati RM, Tateno AF, et al. Rhinovirus C and respiratory exacerbations in children with cystic fibrosis. Emerg Infect Dis 2010; 16: 996–999.
124. Flight WG, Bright-Thomas RJ, Sarran C, et al. The effect of the weather on pulmonary exacerbations and viral infections among adults with cystic fibrosis. Int J Biometeorol 2014; 58: 1845–1851.
125. Ramirez IA, Caverly LL, Kalikin LM, et al. Differential responses to rhinovirus- and influenza-associated pulmonary exacerbations in patients with cystic fibrosis. Ann Am Thorac Soc 2014; 11: 554–561.
126. Collinson J, Nicholson KG, Cancio E, et al. Effects of upper respiratory tract infections in patients with cystic fibrosis. Thorax 1996; 51: 1115–1122.
127. Wang EE, Prober CG, Manson B, et al. Association of respiratory viral infections with pulmonary deterioration in patients with cystic fibrosis. N Engl J Med 1984; 311: 1653–1658.
128. Smyth AR, Smyth RL, Tong CY, et al. Effect of respiratory virus infections including rhinovirus on clinical status in cystic fibrosis. Arch Dis Child 1995; 73: 117–120.
129. Johansen HK, Hoiby N. Seasonal onset of initial colonisation and chronic infection with Pseudomonas aeruginosa in patients with cystic fibrosis in Denmark. Thorax 1992; 47: 109–111.
130. van Ewijk BE, Wolfs TF, Fleer A, et al. High Pseudomonas aeruginosa acquisition rate in CF. Thorax 2006; 61: 641–642.
131. Van Ewijk BE, Wolfs TF, Aerts PC, et al. RSV mediates Pseudomonas aeruginosa binding to cystic fibrosis and normal epithelial cells. Pediatr Res 2007; 61: 398–403.
132. Holt PG, Strickland DH, Sly PD. Virus infection and allergy in the development of asthma: what is the connection? Curr Opin Allergy Clin Immunol 2012; 12: 151–157.
133. Sorkness RL, Szakaly RJ, Rosenthal LA, et al. Viral bronchiolitis in young rats causes small airway lesions that correlate with reduced lung function. Am J Respir Cell Mol Biol 2013; 49: 808–813.
134. Poorisrisak P, Halkjaer LB, Thomsen SF, et al. Causal direction between respiratory syncytial virus bronchiolitis and asthma studied in monozygotic twins. Chest 2010; 138: 338–344.
135. Freymuth F, Vabret A, Dina J, et al. Les virus des bronchiolites aigues [Bronchiolitis viruses]. Arch Pediatr 2010; 17: 1192–1201.
136. 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: 667–672.
137. Lee WM, Lemanske RF Jr, Evans MD, et al. Human rhinovirus species and season of infection determine illness severity. Am J Respir Crit Care Med 2012; 186: 886–891.
138. Palmenberg AC, Rathe JA, Liggett SB. Analysis of the complete genome sequences of human rhinovirus. J Allergy Clin Immunol 2010; 125: 1190–1199.
139. Carroll KN, Gebretsadik T, Minton P, et al. Influence of maternal asthma on the cause and severity of infant acute respiratory tract infections. J Allergy Clin Immunol 2012; 129: 1236–1242.
140. Sigurs N, Aljassim F, Kjellman B, et al. Asthma and allergy patterns over 18 years after severe RSV bronchiolitis in the first year of life. Thorax 2010; 65: 1045–1052.
141. Bacharier LB, Cohen R, Schweiger T, et al. Determinants of asthma after severe respiratory syncytial virus bronchiolitis. J Allergy Clin Immunol 2012; 130: 91–100.
142. Stein RT, Sherrill D, Morgan WJ, et al. Respiratory syncytial virus in early life and risk of wheeze and allergy by age 13 years. Lancet 1999; 354: 541–545.
143. James KM, Gebretsadik T, Escobar GJ, et al. Risk of childhood asthma following infant bronchiolitis during the respiratory syncytial virus season. J Allergy Clin Immunol 2013; 132: 227–229.
144. Kotaniemi-Syrjanen A, Vainionpaa R, Reijonen TM, et al. Rhinovirus-induced wheezing in infancy–the first sign of childhood asthma? J Allergy Clin Immunol 2003; 111: 66–71.
145. Valkonen H, Waris M, Ruohola A, et al. Recurrent wheezing after respiratory syncytial virus or non-respiratory syncytial virus bronchiolitis in infancy: a 3-year follow-up. Allergy 2009; 64: 1359–1365.
146. Midulla F, Pierangeli A, Cangiano G, et al. Rhinovirus bronchiolitis and recurrent wheezing: 1-year follow-up. Eur Respir J 2012; 39: 396–402.
147. 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: 1105–1110.
148. Lemanske RF Jr, Jackson DJ, Gangnon RE, et al. Rhinovirus illnesses during infancy predict subsequent childhood wheezing. J Allergy Clin Immunol 2005; 116: 571–577.
149. Guilbert TW, Singh AM, Danov Z, et al. Decreased lung function after preschool wheezing rhinovirus illnesses in children at risk to develop asthma. J Allergy Clin Immunol 2011; 128: 532–538.
150. Caliskan M, Bochkov YA, Kreiner-Moller E, et al. Rhinovirus wheezing illness and genetic risk of childhood-onset asthma. N Engl J Med 2013; 368: 1398–1407.
151. Raedler D, Illi S, Pinto LA, et al. IL10 polymorphisms influence neonatal immune responses, atopic dermatitis, and wheeze at age 3 years. J Allergy Clin Immunol 2013; 131: 789–796.
152. Jartti T, Kuusipalo H, Vuorinen T, et al. Allergic sensitization is associated with rhinovirus-, but not other virus-, induced wheezing in children. Pediatr Allergy Immunol 2010; 21: 1008–1014.
153. Jackson DJ, Evans MD, Gangnon RE, et al. Evidence for a causal relationship between allergic sensitization and rhinovirus wheezing in early life. Am J Respir Crit Care Med 2012; 185: 281–285.
154. Stern DA, Guerra S, Halonen M, et al. Low IFN-gamma production in the first year of life as a predictor of wheeze during childhood. J Allergy Clin Immunol 2007; 120: 835–841.
155. Sumino K, Tucker J, Shahab M, et al. Antiviral IFN-gamma responses of monocytes at birth predict respiratory tract illness in the first year of life. J Allergy Clin Immunol 2012; 129: 1267–1273.
156. Jackson DJ, Sykes A, Mallia P, et al. Asthma exacerbations: origin, effect, and prevention. J Allergy Clin Immunol 2011; 128: 1165–1174.
157. van der Zalm MM, Uiterwaal CS, Wilbrink B, et al. The influence of neonatal lung function on rhinovirus-associated wheeze. Am J Respir Crit Care Med 2011; 183: 262–267.
158. Chawes BL, Poorisrisak P, Johnston SL, et al. Neonatal bronchial hyperresponsiveness precedes acute severe viral bronchiolitis in infants. J Allergy Clin Immunol 2012; 130: 354–361.
159. Pernet E, Guillemot L, Burgel PR, et al. Pseudomonas aeruginosa eradicates Staphylococcus aureus by manipulating the host immunity. Nat Commun 2014; 5: 5105.
160. Cui L, Morris A, Huang L, et al. The microbiome and the lung. Ann Am Thorac Soc 2014; 11: Suppl. 4, S227–S232.
161. Choi IS, Koh YI. Therapeutic effects of BCG vaccination in adult asthmatic patients: a randomized, controlled trial. Ann Allergy Asthma Immunol 2002; 88: 584–591.