The emerging relationship between the airway microbiota and chronic respiratory disease: clinical implications

References

• Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature444(7122), 1027–1031 (2006).
   PubMed Web of Science ®Google Scholar
• Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature444(7122), 1022–1023 (2006).
   PubMed Web of Science ®Google Scholar
• Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc. Natl Acad. Sci. USA102(31), 11070–11075 (2005).
   PubMed Web of Science ®Google Scholar
• Huang YJ, Nelson CE, Brodie EL et al. Airway microbiota and bronchial hyperresponsiveness in patients with suboptimally controlled asthma. J. Allergy Clin. Immunol.127, 372–381 e1–e3 (2011).
   PubMed Web of Science ®Google Scholar
• Johnston SL, Martin RJ. Chlamydophila pneumoniae and Mycoplasma pneumoniae: a role in asthma pathogenesis? Am. J. Respir. Crit. Care Med.172(9), 1078–1089 (2005).
   PubMed Web of Science ®Google Scholar
• Hahn DL, Dodge RW, Golubjatnikov R. Association of Chlamydia pneumoniae (strain TWAR) infection with wheezing, asthmatic bronchitis, and adult-onset asthma. JAMA266(2), 225–230 (1991).
   PubMed Web of Science ®Google Scholar
• Sirmatel F, Ustunsoy H, Sirmatel O, Akdemir I, Dikensoy O. The relationship between Chlamydia pneumoniae seropositivity and peripheral vascular diseases, acute myocardial infarction and late-onset asthma. Infection31(5), 367–368 (2003).
   Google Scholar
• Yano T, Ichikawa Y, Komatu S, Arai S, Oizumi K. Association of Mycoplasma pneumoniae antigen with initial onset of bronchial asthma. Am. J. Respir. Crit. Care Med.149(5), 1348–1353 (1994).
   PubMed Web of Science ®Google Scholar
• Korppi M, Paldanius M, Hyvarinen A, Nevalainen A, Husman T. Chlamydia pneumoniae and newly diagnosed asthma: a case–control study in 1 to 6-year-old children. Respirology9(2), 255–259 (2004).
   PubMedGoogle Scholar
• Routes JM, Nelson HS, Noda JA, Simon FT. Lack of correlation between Chlamydia pneumoniae antibody titers and adult-onset asthma. J. Allergy Clin. Immunol.105(2 Pt 1), 391–392 (2000).
   PubMed Web of Science ®Google Scholar
• Ten Brinke A, Van Dissel JT, Sterk PJ, Zwinderman AH, Rabe KF, Bel EH. Persistent airflow limitation in adult-onset nonatopic asthma is associated with serologic evidence of Chlamydia pneumoniae infection. J. Allergy Clin. Immunol.107(3), 449–454 (2001).
   PubMed Web of Science ®Google Scholar
• Kocabas A, Avsar M, Hanta I, Koksal F, Kuleci S. Chlamydophila pneumoniae infection in adult asthmatics patients. J. Asthma45(1), 39–43 (2008).
   PubMed Web of Science ®Google Scholar
• Martin RJ, Kraft M, Chu HW, Berns EA, Cassell GH. A link between chronic asthma and chronic infection. J. Allergy Clin. Immunol.107(4), 595–601 (2001).
   PubMed Web of Science ®Google Scholar
• Specjalski K, Jassem E. Chlamydophila pneumoniae, Mycoplasma pneumoniae infections, and asthma control. Allergy Asthma Proc.32(2), 9–17 (2011).
   PubMedGoogle Scholar
• Bisgaard H, Hermansen MN, Buchvald F et al. Childhood asthma after bacterial colonization of the airway in neonates. N. Engl. J. Med.357(15), 1487–1495 (2007).
   PubMed Web of Science ®Google Scholar
• Bisgaard H, Hermansen MN, Bonnelykke K et al. Association of bacteria and viruses with wheezy episodes in young children: prospective birth cohort study. BMJ341, c4978 (2010).
   PubMed Web of Science ®Google Scholar
• 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.178(7), 667–672 (2008).
   PubMed Web of Science ®Google Scholar
• Kotaniemi-Syrjanen A, Vainionpaa R, Reijonen TM, Waris M, Korhonen K, Korppi M. Rhinovirus-induced wheezing in infancy – the first sign of childhood asthma? J. Allergy Clin. Immunol.111(1), 66–71 (2003).
   PubMed Web of Science ®Google Scholar
• 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.119(5), 1105–1110 (2007).
   PubMed Web of Science ®Google Scholar
• 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. Thorax65(12), 1045–1052 (2010).
   PubMed Web of Science ®Google Scholar
• Sigurs N. A cohort of children hospitalised with acute RSV bronchiolitis: impact on later respiratory disease. Paediatr. Respir. Rev.3(3), 177–183 (2002).
   Google Scholar
• Sigurs N, Gustafsson PM, Bjarnason R et al. Severe respiratory syncytial virus bronchiolitis in infancy and asthma and allergy at age 13. Am. J. Respir. Crit. Care Med.171(2), 137–141 (2005).
   PubMed Web of Science ®Google Scholar
• Dulek DE, Peebles RS Jr. Viruses and asthma. Biochim. Biophys. Acta doi:10.1016/j.bbagen.2011.01.012 (2011) (Epub ahead of print).
   PubMedGoogle Scholar
• Garcia-Garcia ML, Calvo C, Casas I et al. Human metapneumovirus bronchiolitis in infancy is an important risk factor for asthma at age 5. Pediatr. Pulmonol.42(5), 458–464 (2007).
   PubMed Web of Science ®Google Scholar
• Murphy TF, Brauer AL, Eschberger K et al.Pseudomonas aeruginosa in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med.177(8), 853–860 (2008).
   PubMed Web of Science ®Google Scholar
• Murphy TF, Brauer AL, Grant BJ, Sethi S. Moraxella catarrhalis in chronic obstructive pulmonary disease: burden of disease and immune response. Am. J. Respir. Crit. Care Med.172(2), 195–199 (2005).
   PubMed Web of Science ®Google Scholar
• Papi A, Bellettato CM, Braccioni F et al. Infections and airway inflammation in chronic obstructive pulmonary disease severe exacerbations. Am. J. Respir. Crit. Care Med.173(10), 1114–1121 (2006).
   PubMed Web of Science ®Google Scholar
• Sethi S, Evans N, Grant BJ, Murphy TF. New strains of bacteria and exacerbations of chronic obstructive pulmonary disease. N. Engl. J. Med.347(7), 465–471 (2002).
   PubMed Web of Science ®Google Scholar
• Sethi S, Wrona C, Eschberger K, Lobbins P, Cai X, Murphy TF. Inflammatory profile of new bacterial strain exacerbations of chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med.177(5), 491–497 (2008).
   PubMed Web of Science ®Google Scholar
• Sethi S, Murphy TF. Infection in the pathogenesis and course of chronic obstructive pulmonary disease. N. Engl. J. Med.359(22), 2355–2365 (2008).
   PubMed Web of Science ®Google Scholar
• Martinez-Solano L, Macia MD, Fajardo A, Oliver A, Martinez JL. Chronic Pseudomonas aeruginosa infection in chronic obstructive pulmonary disease. Clin. Infect. Dis.47(12), 1526–1533 (2008).
   PubMed Web of Science ®Google Scholar
• Rakhimova E, Wiehlmann L, Brauer AL, Sethi S, Murphy TF, Tummler B. Pseudomonas aeruginosa population biology in chronic obstructive pulmonary disease. J. Infect. Dis.200(12), 1928–1935 (2009).
   PubMed Web of Science ®Google Scholar
• Bafadhel M, Mckenna S, Terry S et al. Acute exacerbations of COPD: identification of biological clusters and their biomarkers. Am. J. Respir. Crit. Care Med. doi:201104-0597OCv1 (2011) (Epub ahead of print).
   Google Scholar
• De Serres G, Lampron N, La Forge J et al. Importance of viral and bacterial infections in chronic obstructive pulmonary disease exacerbations. J. Clin. Virol.46(2), 129–133 (2009).
   PubMed Web of Science ®Google Scholar
• Kherad O, Kaiser L, Bridevaux PO et al. Upper-respiratory viral infection, biomarkers, and COPD exacerbations. Chest138(4), 896–904 (2010).
   PubMed Web of Science ®Google Scholar
• Wilkinson TM, Hurst JR, Perera WR, Wilks M, Donaldson GC, Wedzicha JA. Effect of interactions between lower airway bacterial and rhinoviral infection in exacerbations of COPD. Chest129(2), 317–324 (2006).
   PubMed Web of Science ®Google Scholar
• Avadhanula V, Rodriguez CA, Devincenzo JP et al. Respiratory viruses augment the adhesion of bacterial pathogens to respiratory epithelium in a viral species- and cell type-dependent manner. J. Virol.80(4), 1629–1636 (2006).
   PubMed Web of Science ®Google Scholar
• Sajjan US, Jia Y, Newcomb DC et al. H. influenzae potentiates airway epithelial cell responses to rhinovirus by increasing ICAM-1 and TLR3 expression. FASEB J.20(12), 2121–2123 (2006).
   PubMed Web of Science ®Google Scholar
• Soler N, Ewig S, Torres A, Filella X, Gonzalez J, Zaubet A. Airway inflammation and bronchial microbial patterns in patients with stable chronic obstructive pulmonary disease. Eur. Respir. J.14(5), 1015–1022 (1999).
   PubMed Web of Science ®Google Scholar
• Rosell A, Monso E, Soler N et al. Microbiologic determinants of exacerbation in chronic obstructive pulmonary disease. Arch. Intern. Med.165(8), 891–897 (2005).
   PubMed Web of Science ®Google Scholar
• Sethi S, Maloney J, Grove L, Wrona C, Berenson CS. Airway inflammation and bronchial bacterial colonization in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med.173(9), 991–998 (2006).
   PubMed Web of Science ®Google Scholar
• Zhang M, Li Q, Zhang XY, Ding X, Zhu D, Zhou X. 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.29(12), 1487–1493 (2010).
   PubMed Web of Science ®Google Scholar
• Wen Y, Reid DW, Zhang D, Ward C, Wood-Baker R, Walters EH. Assessment of airway inflammation using sputum, BAL, and endobronchial biopsies in current and ex-smokers with established COPD. Int. J. Chron. Obstruct. Pulmon. Dis.5, 327–334 (2010).
   PubMedGoogle Scholar
• Morris A, Sciurba FC, Norris KA. Pneumocystis: a novel pathogen in chronic obstructive pulmonary disease? COPD5(1), 43–51 (2008).
   PubMedGoogle Scholar
• Retamales I, Elliott WM, Meshi B et al. Amplification of inflammation in emphysema and its association with latent adenoviral infection. Am. J. Respir. Crit. Care Med.164(3), 469–473 (2001).
   PubMed Web of Science ®Google Scholar
• Mc Manus TE, Moore JE, Crowe M, Dunbar K, Elborn JS. A comparison of pulmonary exacerbations with single and multiple organisms in patients with cystic fibrosis and chronic Burkholderia cepacia infection. J. Infect.46(1), 56–59 (2003).
   PubMedGoogle Scholar
• Coenye T, Vandamme P, Lipuma JJ. Infection by Ralstonia species in cystic fibrosis patients: identification of R. pickettii and R. mannitolilytica by polymerase chain reaction. Emerg. Infect. Dis.8(7), 692–696 (2002).
   Google Scholar
• Atkinson RM, Lipuma JJ, Rosenbluth DB, Dunne WM Jr. Chronic colonization with Pandoraea apista in cystic fibrosis patients determined by repetitive-element-sequence PCR. J. Clin. Microbiol.44(3), 833–836 (2006).
   PubMed Web of Science ®Google Scholar
• Jorgensen IM, Johansen HK, Frederiksen B et al. Epidemic spread of Pandoraea apista, a new pathogen causing severe lung disease in cystic fibrosis patients. Pediatr. Pulmonol.36(5), 439–446 (2003).
   PubMed Web of Science ®Google Scholar
• Grinwis ME, Sibley CD, Parkins MD, Eshaghurshan CS, Rabin HR, Surette MG. Characterization of Streptococcus milleri group isolates from expectorated sputum of adult patients with cystic fibrosis. J. Clin. Microbiol.48(2), 395–401 (2009).
   Google Scholar
• Parkins MD, Sibley CD, Surette MG, Rabin HR. The Streptococcus milleri group – an unrecognized cause of disease in cystic fibrosis: a case series and literature review. Pediatr. Pulmonol.43(5), 490–497 (2008).
   PubMedGoogle Scholar
• Canton R, Morosini MI, Ballestero S et al. Lung colonization with Enterobacteriaceae producing extended-spectrum β-lactamases in cystic fibrosis patients. Pediatr. Pulmonol.24(3), 213–217 (1997).
   Google Scholar
• De Almeida MB, Zerbinati RM, Tateno AF et al. Rhinovirus C and respiratory exacerbations in children with cystic fibrosis. Emerg. Infect. Dis.16(6), 996–999 (2010).
   PubMed Web of Science ®Google Scholar
• Smyth AR, Smyth RL, Tong CY, Hart CA, Heaf DP. Effect of respiratory virus infections including rhinovirus on clinical status in cystic fibrosis. Arch. Dis. Child.73(2), 117–120 (1995).
   PubMed Web of Science ®Google Scholar
• Wat D, Gelder C, Hibbitts S et al. Is there a role for influenza vaccination in cystic fibrosis? J. Cyst. Fibros.7(1), 85–88 (2008).
   PubMed Web of Science ®Google Scholar
• Chattoraj SS, Ganesan S, Faris A, Comstock A, Lee WM, Sajjan US. Pseudomonas aeruginosa suppresses interferon response to rhinovirus infection in cystic fibrosis, but not in normal bronchial epithelial cells. Infect. Immun.79(10), 4131–4145 (2011).
   PubMed Web of Science ®Google Scholar
• Bik EM, Eckburg PB, Gill SR et al. Molecular analysis of the bacterial microbiota in the human stomach. Proc. Natl Acad. Sci. USA103(3), 732–737 (2006).
   PubMed Web of Science ®Google Scholar
• Dewhirst FE, Chen T, Izard J et al. The human oral microbiome. J. Bacteriol.192(19), 5002–5017 (2010).
   PubMed Web of Science ®Google Scholar
• Eckburg PB, Bik EM, Bernstein CN et al. Diversity of the human intestinal microbial flora. Science308(5728), 1635–1638 (2005).
   PubMed Web of Science ®Google Scholar
• Grice EA, Segre JA. The skin microbiome. Nat. Rev. Microbiol.9(4), 244–253 (2011).
   PubMed Web of Science ®Google Scholar
• Brodie EL, Desantis TZ, Parker JP, Zubietta IX, Piceno YM, Andersen GL. Urban aerosols harbor diverse and dynamic bacterial populations. Proc. Natl Acad. Sci. USA104(1), 299–304 (2007).
   PubMed Web of Science ®Google Scholar
• Desantis TZ, Brodie EL, Moberg JP, Zubieta IX, Piceno YM, Andersen GL. High-density universal 16S rRNA microarray analysis reveals broader diversity than typical clone library when sampling the environment. Microb. Ecol.53(3), 371–383 (2007).
   PubMed Web of Science ®Google Scholar
• Lemos LN, Fulthorpe RR, Triplett EW, Roesch LF. Rethinking microbial diversity analysis in the high throughput sequencing era. J. Microbiol. Methods86(1), 42–51 (2011).
   PubMed Web of Science ®Google Scholar
• Petrosino JF, Highlander S, Luna RA, Gibbs RA, Versalovic J. Metagenomic pyrosequencing and microbial identification. Clin. Chem.55(5), 856–866 (2009).
   PubMed Web of Science ®Google Scholar
• Van Den Bogert B, De Vos WM, Zoetendal EG, Kleerebezem M. Microarray analysis and barcoded pyrosequencing provide consistent microbial profiles depending on the source of human intestinal samples. Appl. Environ. Microbiol.77(6), 2071–2080 (2011).
   PubMedGoogle Scholar
• Ghannoum MA, Jurevic RJ, Mukherjee PK et al. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog.6(1), e1000713 (2010).
   PubMed Web of Science ®Google Scholar
• Kistler A, Avila PC, Rouskin S et al. Pan-viral screening of respiratory tract infections in adults with and without asthma reveals unexpected human coronavirus and human rhinovirus diversity. J. Infect. Dis.196(6), 817–825 (2007).
   PubMed Web of Science ®Google Scholar
• Paulino LC, Tseng CH, Strober BE, Blaser MJ. Molecular analysis of fungal microbiota in samples from healthy human skin and psoriatic lesions. J. Clin. Microbiol.44(8), 2933–2941 (2006).
   PubMed Web of Science ®Google Scholar
• Wang D, Coscoy L, Zylberberg M et al. Microarray-based detection and genotyping of viral pathogens. Proc. Natl Acad. Sci. USA99(24), 15687–15692 (2002).
   PubMed Web of Science ®Google Scholar
• Reyes A, Haynes M, Hanson N et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature466(7304), 334–338 (2010).
   PubMed Web of Science ®Google Scholar
• Dethlefsen L, Mcfall-Ngai M, Relman DA. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature449(7164), 811–818 (2007).
   PubMed Web of Science ®Google Scholar
• Fujimura KE, Slusher NA, Cabana MD, Lynch SV. Role of the gut microbiota in defining human health. Expert Rev. Anti Infect. Ther.8(4), 435–454 (2010).
   PubMed Web of Science ®Google Scholar
• Wade WG. Has the use of molecular methods for the characterization of the human oral microbiome changed our understanding of the role of bacteria in the pathogenesis of periodontal disease? J. Clin. Periodontol.38(Suppl. 11), 7–16 (2011).
   Google Scholar
• Lemon KP, Klepac-Ceraj V, Schiffer HK, Brodie EL, Lynch SV, Kolter R. Comparative analyses of the bacterial microbiota of the human nostril and oropharynx. MBio1(3), e00129-10 (2010).
   Google Scholar
• Zaura E, Keijser BJ, Huse SM, Crielaard W. Defining the healthy ‘core microbiome’ of oral microbial communities. BMC Microbiol.9, 259 (2009).
   PubMed Web of Science ®Google Scholar
• Arumugam M, Raes J, Pelletier E et al. Enterotypes of the human gut microbiome. Nature473(7346), 174–180 (2011).
   PubMed Web of Science ®Google Scholar
• Norris KA, Morris A. Pneumocystis infection and the pathogenesis of chronic obstructive pulmonary disease. Immunol. Res.50(2–3), 175–180 (2011).
   Google Scholar
• Morris A, Alexander T, Radhi S et al. Airway obstruction is increased in pneumocystis-colonized human immunodeficiency virus-infected outpatients. J. Clin. Microbiol.47(11), 3773–3776 (2009).
   PubMed Web of Science ®Google Scholar
• Reihill JA, Moore JE, Elborn JS, Ennis M. Effect of Aspergillus fumigatus and Candida albicans on pro-inflammatory response in cystic fibrosis epithelium. J. Cyst. Fibros. doi:10.1016/j.jcf.2011.06.006 (2011) (Epub ahead of print).
   Google Scholar
• Muller FM, Seidler M. Characteristics of pathogenic fungi and antifungal therapy in cystic fibrosis. Expert Rev. Anti Infect. Ther.8(8), 957–964 (2010).
   PubMed Web of Science ®Google Scholar
• Horre R, Marklein G, Siekmeier R, Reiffert SM. Detection of hyphomycetes in the upper respiratory tract of patients with cystic fibrosis. Mycoses doi:10.1111/j.1439-0507.2010.01897.x (2010) (Epub ahead of print).
   Google Scholar
• Charlson ES, Bittinger K, Haas AR et al. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am. J. Respir. Crit. Care Med. doi:201104-0655OCv2 (2011) (Epub ahead of print).
   Google Scholar
• Hilty M, Burke C, Pedro H et al. Disordered microbial communities in asthmatic airways. PLoS One5(1), e8578 (2010).
   PubMed Web of Science ®Google Scholar
• Charlson ES, Chen J, Custers-Allen R et al. Disordered microbial communities in the upper respiratory tract of cigarette smokers. PLoS One5(12), e15216 (2010).
   PubMed Web of Science ®Google Scholar
• Henriksson G, Helgeland L, Midtvedt T, Stierna P, Brandtzaeg P. Immune response to Mycoplasma pulmonis in nasal mucosa is modulated by the normal microbiota. Am. J. Respir. Cell Mol. Biol.31(6), 657–662 (2004).
   PubMed Web of Science ®Google Scholar
• Ichinohe T, Pang IK, Kumamoto Y et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl Acad. Sci. USA108(13), 5354–5359 (2011).
   PubMed Web of Science ®Google Scholar
• Erb-Downward JR, Thompson DL, Han MK et al. Analysis of the lung microbiome in the ‘healthy’ smoker and in COPD. PLoS One6(2), e16384 (2011).
   PubMed Web of Science ®Google Scholar
• Huang YJ, Kim E, Cox MJ et al. A persistent and diverse airway microbiota present during chronic obstructive pulmonary disease exacerbations. OMICS14(1), 9–59 (2010).
   PubMed Web of Science ®Google Scholar
• Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol.8(6), 411–420 (2008).
   PubMed Web of Science ®Google Scholar
• Rogers GB, Hart CA, Mason JR, Hughes M, Walshaw MJ, Bruce KD. Bacterial diversity in cases of lung infection in cystic fibrosis patients: 16S ribosomal DNA (rDNA) length heterogeneity PCR and 16S rDNA terminal restriction fragment length polymorphism profiling. J. Clin. Microbiol.41(8), 3548–3558 (2003).
   PubMedGoogle Scholar
• Rogers GB, Carroll MP, Serisier DJ et al. Bacterial activity in cystic fibrosis lung infections. Respir. Res.6, 49 (2005).
   PubMed Web of Science ®Google Scholar
• Rogers GB, Carroll MP, Serisier DJ, Hockey PM, Jones G, Bruce KD. Characterization of bacterial community diversity in cystic fibrosis lung infections by use of 16s ribosomal DNA terminal restriction fragment length polymorphism profiling. J. Clin. Microbiol.42(11), 5176–5183 (2004).
   PubMed Web of Science ®Google Scholar
• Harris JK, De Groote MA, Sagel SD et al. Molecular identification of bacteria in bronchoalveolar lavage fluid from children with cystic fibrosis. Proc. Natl Acad. Sci. USA104(51), 20529–20533 (2007).
   PubMed Web of Science ®Google Scholar
• 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.12(5), 1293–1303 (2010).
   PubMed Web of Science ®Google Scholar
• Cox MJ, Allgaier M, Taylor B et al. Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PLoS One5(6), e11044 (2010).
   PubMed Web of Science ®Google Scholar
• Duan K, Dammel C, Stein J, Rabin H, Surette MG. Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol. Microbiol.50(5), 1477–1491 (2003).
   PubMed Web of Science ®Google Scholar
• Sibley CD, Duan K, Fischer C et al. Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections. PLoS Pathog.4(10), e1000184 (2008).
   PubMed Web of Science ®Google Scholar
• Høiby N, Ciofu O, Johansen HK et al. The clinical impact of bacterial biofilms. Int. J. Oral Sci.3(2), 55–65 (2011).
   PubMed Web of Science ®Google Scholar
• Campos J, Roman F, Georgiou M et al. Long-term persistence of ciprofloxacin-resistant Haemophilus influenzae in patients with cystic fibrosis. J. Infect. Dis.174(6), 1345–1347 (1996).
   PubMed Web of Science ®Google Scholar
• Hoiby N. Epidemiological investigations of the respiratory tract bacteriology in patients with cystic fibrosis. Acta Pathol. Microbiol. Scand. B Microbiol. Immunol.82(4), 541–550 (1974).
   Google Scholar
• Clode FE, Metherell LA, Pitt TL. Nosocomial acquisition of Burkholderia gladioli in patients with cystic fibrosis. Am. J. Respir. Crit. Care Med.160(1), 374–375 (1999).
   Google Scholar
• Yang JH, Spilker T, LiPuma JJ. Simultaneous coinfection by multiple strains during Burkholderia cepacia complex infection in cystic fibrosis. Diagn. Microbiol. Infect. Dis.54(2), 95–98 (2006).
   Google Scholar
• Drevinek P, Mahenthiralingam E. Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin. Microbiol. Infect.16(7), 821–830 (2010).
   PubMed Web of Science ®Google Scholar
• Gibson RL, Burns JL, Ramsey BW. Pathophysiology and management of pulmonary infections in cystic fibrosis. Am. J. Respir. Crit. Care Med.168(8), 918–951 (2003).
   PubMed Web of Science ®Google Scholar
• Lambiase A, Catania MR, Del Pezzo M et al.Achromobacter xylosoxidans respiratory tract infection in cystic fibrosis patients. Eur. J. Clin. Microbiol. Infect. Dis.30(8), 973–980 (2011).
   PubMed Web of Science ®Google Scholar
• Esther CR Jr, Esserman DA, Gilligan P, Kerr A, Noone PG. Chronic Mycobacterium abscessus infection and lung function decline in cystic fibrosis. J. Cyst. Fibros.9(2), 117–123 (2010).
   PubMed Web of Science ®Google Scholar
• Bauernfeind A, Bertele RM, Harms K et al. Qualitative and quantitative microbiological analysis of sputa of 102 patients with cystic fibrosis. Infection15(4), 270–277 (1987).
   PubMedGoogle Scholar
• Del Campo R, Morosini MI, De La Pedrosa EG et al. Population structure, antimicrobial resistance, and mutation frequencies of Streptococcus pneumoniae isolates from cystic fibrosis patients. J. Clin. Microbiol.43(5), 2207–2214 (2005).
   PubMed Web of Science ®Google Scholar