Cystic fibrosis respiratory microbiota: unraveling complexity to inform clinical practice

References

• Salsgiver EL, Fink AK, Knapp EA, et al. Changing epidemiology of the respiratory bacteriology of patients with cystic fibrosis. Chest. 2016;149:390–400.
   PubMed Web of Science ®Google Scholar
• Cystic Fibrosis Foundation. Patient registry annual data report. 2016.
   Google Scholar
• Sanders DB, Bittner RC, Rosenfeld M, et al. Failure to recover to baseline pulmonary function after cystic fibrosis pulmonary exacerbation. Am J Respir Crit Care Med. 2010;182:627–632.
   PubMed Web of Science ®Google Scholar
• Smith AL, Fiel SB, Mayer-Hamblett N, et al. Susceptibility testing of Pseudomonas aeruginosa isolates and clinical response to parenteral antibiotic administration lack of association in cystic fibrosis. Chest. 2003;123:1495–1502.
   PubMed Web of Science ®Google Scholar
• Zemanick ET, Wagner BD, Harris JK, et al. Pulmonary exacerbations in cystic fibrosis with negative bacterial cultures. Pediatr Pulmonol. 2010;45:569–577.
   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 One. 2010;5:e11044.
   PubMed Web of Science ®Google Scholar
• Coburn B, Wang PW, Diaz Caballero J, et al. Lung microbiota across age and disease stage in cystic fibrosis. Sci Rep. 2015;5:10241.
   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 U S A. 2007;104:20529–20533.
   PubMed Web of Science ®Google Scholar
• Zemanick ET, Wagner BD, Robertson CE, et al. Airway microbiota across age and disease spectrum in cystic fibrosis. Eur Respir J. 2017;50:1700832.
   PubMed Web of Science ®Google Scholar
• Mahboubi MA, Carmody LA, Foster BK, et al. Culture-based and culture-independent bacteriologic analysis of cystic fibrosis respiratory specimens. J Clin Microbiol. 2015;54:613–619.
   PubMed Web of Science ®Google Scholar
• Venkataraman A, Bassis CM, Beck JM, et al. Application of a neutral community model to assess structuring of the human lung microbiome, MBio. 2015;6:e02284-14.
   Web of Science ®Google Scholar
• Dickson RP, Erb-Downward JR, Freeman CM, et al. Bacterial topography of the healthy human lower respiratory tract. MBio. 2017;8:e02287–16.
   PubMed Web of Science ®Google Scholar
• Bassis CM, Erb-Downward JR, Dickson RP, et al. Analysis of the upper respiratory tract microbiotas as the source of the lung and gastric microbiotas in healthy individuals. MBio. 2015;6:e00037.
   PubMed Web of Science ®Google Scholar
• Brown PS, Pope CE, Marsh RL, et al. Directly sampling the lung of a young child with cystic fibrosis reveals diverse microbiota. Ann Am Thorac Soc. 2014;11:1049–1055.
   PubMedGoogle Scholar
• Pittman JE, Wylie KM, Akers K, et al. Association of antibiotics, airway microbiome and inflammation in infants with cystic fibrosis. Ann Am Thorac Soc. 2017;14:1548–1555.
   PubMed Web of Science ®Google Scholar
• Frayman KB, Armstrong DS, Carzino R, et al. The lower airway microbiota in early cystic fibrosis lung disease: a longitudinal analysis. Thorax. 2017;72:1104–1112.
   PubMed Web of Science ®Google Scholar
• Zemanick ET, Wagner BD, Robertson CE, et al. Assessment of airway microbiota and inflammation in cystic fibrosis using multiple sampling methods. Ann Am Thorac Soc. 2015;12:221–229.
   PubMed Web of Science ®Google Scholar
• Muhlebach MS, Zorn BT, Esther CR, et al. Initial acquisition and succession of the cystic fibrosis lung microbiome is associated with disease progression in infants and preschool children. PLoS Pathog. 2018;14:e1006798.
   PubMed Web of Science ®Google Scholar
• Hoen AG, Li J, Moulton LA, et al. Associations between gut microbial colonization in early life and respiratory outcomes in cystic fibrosis. J Pediatr. 2015;167:138–147.
   PubMed Web of Science ®Google Scholar
• Madan JC, Koestler DC, Stanton BA, et al. Serial analysis of the gut and respiratory microbiome in cystic fibrosis in infancy: interaction between intestinal and respiratory tracts and impact of nutritional exposures. MBio. 2012;3:e00251-12.
   Web of Science ®Google Scholar
• Tunney MM, Klem ER, Fodor AA, et al. Use of culture and molecular analysis to determine the effect of antibiotic treatment on microbial community diversity and abundance during exacerbation in patients with cystic fibrosis. Thorax. 2011;66:579–584.
   PubMed Web of Science ®Google Scholar
• Worlitzsch D, Rintelen C, Bohm K, et al. Antibiotic-resistant obligate anaerobes during exacerbations of cystic fibrosis patients. Clin Microbiol Infect. 2009;15:454–460.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Rogers GB, Hart CA, Mason JR, et al. 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. 2003;41:3548–3558.
   PubMed Web of Science ®Google Scholar
• Caverly LJ, Zhao J, LiPuma JJ. Cystic fibrosis lung microbiome: opportunities to reconsider management of airway infection. Pediatr Pulmonol. 2015;50:S31–8.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Carmody LA, Zhao J, Schloss PD, et al. Changes in cystic fibrosis airway microbiota at pulmonary exacerbation. Ann Am Thorac Soc. 2013;10:179–187.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Deschaght P, Schelstraete P, Van Simaey L, et al. Is the improvement of CF patients, hospitalized for pulmonary exacerbation, correlated to a decrease in bacterial load? PLoS One. 2013;8:e79010.
   PubMed Web of Science ®Google Scholar
• Carmody LA, Caverly LJ, Foster BK, et al. Fluctuations in airway bacterial communities associated with clinical states and disease stages in cystic fibrosis. PLoS One. 2018;13:e0194060.
   PubMed Web of Science ®Google Scholar
• Konstan MW, Wagener JS, VanDevanter DR. Characterizing aggressiveness and predicting future progression of CF lung disease. J Cyst Fibros. 2009;8:S15–S19.
   PubMedGoogle Scholar
• Ranganathan SC, Hall GL, Sly PD, et al. Early lung disease in infants and pre-school children with cystic fibrosis: what have we learnt and what should we do about it? Am J Respir Crit Care Med. 2017;195:1567–1575.
   PubMed Web of Science ®Google Scholar
• Laguna TA, Wagner BD, Williams CB, et al. Airway microbiota in bronchoalveolar lavage fluid from clinically well infants with cystic fibrosis. PLoS One. 2016;11:e0167649.
   PubMed Web of Science ®Google Scholar
• Davis SD, Ratjen F, Brumback LC, et al. Infant lung function tests as endpoints in the ISIS multicenter clinical trial in cystic fibrosis. J Cyst Fibros. 2016;15:386–391.
   PubMed Web of Science ®Google Scholar
• Sibley CD, Parkins MD, Rabin HR, et al. A polymicrobial perspective of pulmonary infections exposes an enigmatic pathogen in cystic fibrosis patients. Proc Natl Acad Sci USA. 2008;105:15070–15075.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Whiteson KL, Meinardi S, Lim YW, et al. Breath gas metabolites and bacterial metagenomes from cystic fibrosis airways indicate active pH neutral 2,3-butanedione fermentation. ISME J. 2014;8:1247–1258.
   PubMed Web of Science ®Google Scholar
• Lim YW, Schmieder R, Haynes M, et al. Mechanistic model of Rothia mucilaginosa adaptation toward persistence in the CF lung, based on a genome reconstructed from metagenomic data. PLoS One. 2013;8:e64285.
   PubMed Web of Science ®Google Scholar
• Quinn RA, Whiteson K, Lim YW, et al. Ecological networking of cystic fibrosis lung infections, NPJ Biofilms Microbiomes. 2016;2.
   PubMed Web of Science ®Google Scholar
• Conrad D, Haynes M, Salamon P, et al. Cystic fibrosis therapy: A community ecology perspective. Am J Respir Cell Mol Biol. 2013;48:150–156.
   PubMed Web of Science ®Google Scholar
• Quinn RA, Whiteson K, Lim YW, et al. A Winogradsky-based culture system shows an association between microbial fermentation and cystic fibrosis exacerbation. ISME J. 2015;9:1052.
   PubMed Web of Science ®Google Scholar
• Paganin P, Fiscarelli EV, Tuccio V, et al. Changes in cystic fibrosis airway microbial community associated with a severe decline in lung function. PLoS One. 2015;10:e0124348.
   PubMedGoogle Scholar
• Twomey KB, Alston M, An SQ, et al. Microbiota and metabolite profiling reveal specific alterations in bacterial community structure and environment in the cystic fibrosis airway during exacerbation. PLoS One. 2013;8:e82432.
   PubMed Web of Science ®Google Scholar
• Flynn JM, Niccum D, Dunitz JM, et al. Evidence and role for bacterial mucin degradation in cystic fibrosis airway disease. PLoS Pathog. 2016;12:1–21.
   Web of Science ®Google Scholar
• Mirković B, Murray MA, Lavelle GM, et al. The role of short-chain fatty acids, produced by anaerobic bacteria, in the cystic fibrosis airway. Am J Respir Crit Care Med. 2015;192:1314–1324.
   PubMed Web of Science ®Google Scholar
• Whiley RA, Fleming EV, Makhija R, et al. Environment and colonisation sequence are key parameters driving cooperation and competition between Pseudomonas aeruginosa cystic fibrosis strains and oral commensal streptococci. PLoS One. 2015;10:e0115513.
   Web of Science ®Google Scholar
• Gao B, Gallagher T, Zhang Y, et al. Tracking polymicrobial metabolism in cystic fibrosis airways: Pseudomonas aeruginosa metabolism and physiology are influenced by Rothia mucilaginosa-derived metabolites. mSphere. 2018;3:e00151–18.
   PubMed Web of Science ®Google Scholar
• Stokell JR, Gharaibeh RZ, Hamp TJ, et al. Analysis of changes in diversity and abundance of the microbial community in a cystic fibrosis patient over a multiyear period. J Clin Microbiol. 2015;53:237–247.
   PubMed Web of Science ®Google Scholar
• Carmody LA, Zhao J, Kalikin LM, et al. The daily dynamics of cystic fibrosis airway microbiota during clinical stability and at exacerbation. Microbiome. 2015;3:12.
   PubMed Web of Science ®Google Scholar
• Whelan FJ, Heirali AA, Rossi L, et al. Longitudinal sampling of the lung microbiota in individuals with cystic fibrosis. PLoS One. 2017;12:e0172811.
   PubMed Web of Science ®Google Scholar
• Zhao J, Murray S, LiPuma JJ. Modeling the impact of antibiotic exposure on human microbiota. Sci Rep. 2014;4:4345.
   PubMed Web of Science ®Google Scholar
• Mika M, Korten I, Qi W, et al. The nasal microbiota in infants with cystic fibrosis in the first year of life: a prospective cohort study. Lancet Respir Med. 2016;4:627–635.
   PubMed Web of Science ®Google Scholar
• Prevaes SMPJ, De Winter-De Groot KM, Janssens HM, et al. Development of the nasopharyngeal microbiota in infants with cystic fibrosis. Am J Respir Crit Care Med. 2016;193:504–515.
   PubMed Web of Science ®Google Scholar
• Riaz SP, Linklater KM, Page R, et al. Recent trends in resection rates among non-small cell lung cancer patients in England. Thorax. 2012;67:811–814.
   PubMed Web of Science ®Google Scholar
• Smith DJ, Badrick AC, Zakrzewski M, et al. Pyrosequencing reveals transient cystic fibrosis lung microbiome changes with intravenous antibiotics. Eur Respir J. 2014;44:922–930.
   PubMed Web of Science ®Google Scholar
• Peleg AY, Choo JM, Langan KM, et al. Antibiotic exposure and interpersonal variance mask the effect of ivacaftor on respiratory microbiota composition. Journal of Cystic Fibrosis. 2018;17:50–56.
   PubMed Web of Science ®Google Scholar
• Hogan DA, Willger SD, Dolben EL, et al. Analysis of lung microbiota in bronchoalveolar lavage, protected brush and sputum samples from subjects with mild-to-moderate cystic fibrosis lung disease. PLoS One. 2016;11:e0149998.
   PubMed Web of Science ®Google Scholar
• Filkins LM, Graber JA, Olson DG, et al. Coculture of Staphylococcus aureus with Pseudomonas aeruginosa drives S. Aureus towards fermentative metabolism and reduced viability in a cystic fibrosis model. J Bacteriol. 2015;197:2252–2264.
   PubMed Web of Science ®Google Scholar
• Sherrard LJ, McGrath SJ, McIlreavey L, et al. Production of extended-spectrum beta-lactamases and the potential indirect pathogenic role of Prevotella isolates from the cystic fibrosis respiratory microbiota. Int J Antimicrob Agents. 2015;47:140–145.
   PubMed Web of Science ®Google Scholar
• Jorth P, Staudinger BJ, Wu X, et al. Regional isolation drives bacterial diversification within cystic fibrosis lungs. Cell Host Microbe. 2015;18:307–319.
   PubMed Web of Science ®Google Scholar
• Kopf SH, Sessions AL, Cowley ES, et al. Trace incorporation of heavy water reveals slow and heterogeneous pathogen growth rates in cystic fibrosis sputum. Proc Natl Acad Sci USA. 2016;113:E110–6.
   PubMed Web of Science ®Google Scholar
• Cowley ES, Kopf SH, LaRiviere A, et al. Pediatric cystic fibrosis sputum can be chemically dynamic, anoxic, and extremely reduced due to hydrogen sulfide formation. MBio. 2015;6:e00767.
   PubMed Web of Science ®Google Scholar
• Quinn RA, Navas-Molina JA, Hyde ER, et al. From sample to multi-omics conclusions in under 48 hours. mSystems. 2016;1:e00038–16.
   PubMed Web of Science ®Google Scholar
• Heirali AA, Workentine ML, Acosta N, et al. The effects of inhaled aztreonam on the cystic fibrosis lung microbiome. Microbiome. 2017;5.
   PubMed Web of Science ®Google Scholar
• Bernarde C, Keravec M, Mounier J, et al. Impact of the CFTR-Potentiator ivacaftor on airway microbiota in cystic fibrosis patients carrying a G551D mutation. PLoS One. 2015;10:e0124124.
   PubMed Web of Science ®Google Scholar