Association of antibiotics, airway microbiome, and inflammation in infants with cystic fibrosis

Annals of the American Thoracic Society

Volumn 14, Issue 10, 2017, Pages 1548-1555

  Pittman, Jessica E ^a   Wylie, Kristine M ^a   Akers, Kathryn ^a   Storch, Gregory A ^a   Hatch, Joseph ^b   Quante, Jane ^a   Frayman, Katherine B ^c,d,e   Clarke, Nadeene ^c,d,e   Davis, Miriam ^b   Stick, Stephen M ^f,g,h   Hall, Graham L ^f,g,i   Montgomery, Gregory ^b   Ranganathan, Sarath ^c,d,e   Davis, Stephanie D ^b   Ferkol, Thomas W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^e ROYAL CHILDREN'S HOSPITAL   (Australia)

^f UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^g UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^h PRINCESS MARGARET HOSPITAL FOR CHILDREN   (Australia)

ⁱ CURTIN UNIVERSITY   (Australia)

Author keywords

Bacterial infection; Cystic fibrosis; Microbiota; Pediatric lung disease inflammation; Respiratory infection

Indexed keywords

ANTIBIOTIC AGENT; BACTERIAL DNA; INTERLEUKIN 8; LEUKOCYTE ELASTASE; RNA 16S; BIOLOGICAL MARKER; IL8 PROTEIN, HUMAN;

ACTINOMYCES; ANTIBIOTIC PROPHYLAXIS; ARTICLE; BACILLUS; BACTERIAL FLORA; BACTERIAL LOAD; BACTERIUM CULTURE; BRADYRHIZOBIUM; BRONCHOSCOPY; CAMPYLOBACTER; CLINICAL ARTICLE; CUPRIAVIDUS; CYSTIC FIBROSIS; DISEASE ASSOCIATION; ENTEROCOCCUS; FEMALE; FUSOBACTERIUM; GEMELLA; GRANULICATELLA; HAEMOPHILUS; HUMAN; INFANT; LACTOBACILLUS; LEPTOTRICHIA; LUNG LAVAGE; MALE; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MORAXELLA; NEISSERIA; NEUTROPHIL COUNT; NONHUMAN; OBSERVATIONAL STUDY; PORPHYROMONAS; PREVOTELLA; PROPIONIBACTERIUM; PROSPECTIVE STUDY; PSEUDOMONAS; RESPIRATORY TRACT INFLAMMATION; RHIZOBIUM; ROTHIA; STAPHYLOCOCCUS; STENOTROPHOMONAS; STREPTOCOCCUS; VEILLONELLA; AUSTRALIA; BACTERIUM; BRONCHOALVEOLAR LAVAGE FLUID; CLINICAL TRIAL; COMPLICATION; INFLAMMATION; ISOLATION AND PURIFICATION; LEUKOCYTE COUNT; METABOLISM; MICROBIOLOGY; MICROFLORA; MISSOURI; MULTICENTER STUDY; NEUTROPHIL; RESPIRATORY SYSTEM; STATISTICAL MODEL;

ANTIBIOTIC PROPHYLAXIS; AUSTRALIA; BACTERIA; BIOMARKERS; BRONCHOALVEOLAR LAVAGE FLUID; CYSTIC FIBROSIS; FEMALE; HUMANS; INFANT; INFLAMMATION; INTERLEUKIN-8; LEUKOCYTE COUNT; LEUKOCYTE ELASTASE; LINEAR MODELS; MALE; MICROBIOTA; MISSOURI; NEUTROPHILS; PROSPECTIVE STUDIES; RESPIRATORY SYSTEM;

EID: 85030472724     PISSN: 23256621     EISSN: None     Source Type: Journal    
DOI: 10.1513/AnnalsATS.201702-121OC     Document Type: Article

References (33)

1. Pittman JE, Ferkol TW. The evolution of cystic fibrosis care. Chest 2015;148:533–542.
2. Martin TR. Neutrophils and lung injury: getting it right. J Clin Invest 2002;110:1603–1605.
3. Pillarisetti N, Williamson E, Linnane B, Skoric B, Robertson CF, Robinson P, Massie J, Hall GL, Sly P, Stick S, et al.; Australian Respiratory Early Surveillance Team for Cystic Fibrosis (AREST CF). Infection, inflammation, and lung function decline in infants with cystic fibrosis. Am J Respir Crit Care Med 2011;184:75–81.
4. Sly PD, Gangell CL, Chen L, Ware RS, Ranganathan S, Mott LS, Murray CP, Stick SM, Investigators AC; AREST CF Investigators. Risk factors for bronchiectasis in children with cystic fibrosis. N Engl J Med 2013; 368:1963–1970.
5. Simpson SJ, Ranganathan S, Park J, Turkovic L, Robins-Browne RM, Skoric B, Ramsey KA, Rosenow T, Banton GL, Berry L, et al.; AREST CF. Progressive ventilation inhomogeneity in infants with cystic fibrosis after pulmonary infection. Eur Respir J 2015;46:1680–1690.
6. Ramsey KA, Ranganathan S, Park J, Skoric B, Adams AM, Simpson SJ, Robins-Browne RM, Franklin PJ, de Klerk NH, Sly PD, et al.; AREST CF. Early respiratory infection is associated with reduced spirometry in children with cystic fibrosis. Am J Respir Crit Care Med 2014;190:1111–1116.
7. Li Z, Kosorok MR, Farrell PM, Laxova A, West SE, Green CG, Collins J, Rock MJ, Splaingard ML. Longitudinal development of mucoid Pseudomonas aeruginosa infection and lung disease progression in children with cystic fibrosis. JAMA 2005;293:581–588.
8. Lipuma JJ. The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev 2010;23:299–323.
9. Blainey PC, Milla CE, Cornfield DN, Quake SR. Quantitative analysis of the human airway microbial ecology reveals a pervasive signature for cystic fibrosis. Sci Transl Med 2012;4:153ra130.
10. Mahenthiralingam E. Emerging cystic fibrosis pathogens and the microbiome. Paediatr Respir Rev 2014;15:13–15.
11. Fodor AA, Klem ER, Gilpin DF, Elborn JS, Boucher RC, Tunney MM, Wolfgang MC. 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.
12. Surette MG. The cystic fibrosis lung microbiome. Ann Am Thorac Soc 2014;11:S61–S65.
13. Zhao J, Schloss PD, Kalikin LM, Carmody LA, Foster BK, Petrosino JF, Cavalcoli JD, VanDevanter DR, Murray S, Li JZ, et al. Decade-long bacterial community dynamics in cystic fibrosis airways. Proc Natl Acad Sci USA 2012;109:5809–5814.
14. Coburn B, Wang PW, Diaz Caballero J, Clark ST, Brahma V, Donaldson S, Zhang Y, Surendra A, Gong Y, Elizabeth Tullis D, et al. Lung microbiota across age and disease stage in cystic fibrosis. Sci Rep 2015;5:10241.
15. Paganin P, Fiscarelli EV, Tuccio V, Chiancianesi M, Bacci G, Morelli P, Dolce D, Dalmastri C, De Alessandri A, Lucidi V, et al. Changes in cystic fibrosis airway microbial community associated with a severe decline in lung function. PLoS One 2015;10:e0124348.
16. Renwick J, McNally P, John B, DeSantis T, Linnane B, Murphy P; SHIELD CF. The microbial community of the cystic fibrosis airway is disrupted in early life. PLoS One 2014;9:e109798.
17. Mika M, Korten I, Qi W, Regamey N, Frey U, Casaulta C, Latzin P, Hilty M; SCILD study group. 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.
18. Frayman KB, Armstrong DS, Carzino R, Ferkol TW, Grimwood K, Storch GA, Teo SM, Wylie KM, Ranganathan SC. The lower airway microbiota in early cystic fibrosis lung disease: a longitudinal analysis. Thorax [online ahead of print] 9 Mar 2017; DOI: 10.1136/ thoraxjnl-2016-209279.
19. Pittman JE, Cutting G, Davis SD, Ferkol T, Boucher R. Cystic fibrosis: NHLBI Workshop on the Primary Prevention of Chronic Lung Diseases. Ann Am Thorac Soc 2014;11:S161–S168.
20. Laufer AS, Metlay JP, Gent JF, Fennie KP, Kong Y, Pettigrew MM. Microbial communities of the upper respiratory tract and otitis media in children. MBio 2011;2:e00245–e10.
21. Vael C, Desager K. The importance of the development of the intestinal microbiota in infancy. Curr Opin Pediatr 2009;21:794–800.
22. Heeckeren A, Walenga R, Konstan MW, Bonfield T, Davis PB, Ferkol T. Excessive inflammatory response of cystic fibrosis mice to bronchopulmonary infection with Pseudomonas aeruginosa. J Clin Invest 1997;100:2810–2815.
23. Rennard SI, Basset G, Lecossier D, O’Donnell KM, Pinkston P, Martin PG, Crystal RG. Estimation of volume of epithelial lining fluid recovered by lavage using urea as marker of dilution. J Appl Physiol 1985;1986:532–538.
24. Chen DL, Ferkol TW, Mintun MA, Pittman JE, Rosenbluth DB, Schuster DP. Quantifying pulmonary inflammation in cystic fibrosis with positron emission tomography. Am J Respir Crit Care Med 2006;173:1363–1369.
25. Liu CM, Aziz M, Kachur S, Hsueh PR, Huang YT, Keim P, Price LB. BactQuant: an enhanced broad-coverage bacterial quantitative real-time PCR assay. BMC Microbiol 2012;12:56.
26. Group JCHMPDGW; Jumpstart Consortium Human Microbiome Project Data Generation Working Group. Evaluation of 16S rDNA-based community profiling for human microbiome research. PLoS One 2012;7:e39315.
27. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007;73:5261–5267.
28. Roberts D. labdsv: ordination and multivariate analysis for ecology. R package version 1.8–0. Available from: https://cran.r-project.org/package=labdsv
29. Adler D, Murdoch D. rgl: 3D visualization using OpenGL. R package version 0.95.1441. Available from: https://cran.r-project.org/package=rgl.
30. White JR, Nagarajan N, Pop M. Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLOS Comput Biol 2009;5:e1000352.
31. Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, Turner P, Parkhill J, Loman NJ, Walker AW. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 2014;12:87.
32. Boutin S, Graeber SY, Weitnauer M, Panitz J, Stahl M, Clausznitzer D, Kaderali L, Einarsson G, Tunney MM, Elborn JS, et al. Comparison of microbiomes from different niches of upper and lower airways in children and adolescents with cystic fibrosis. PLoS One 2015;10:e0116029.
33. Smith DJ, Badrick AC, Zakrzewski M, Krause L, Bell SC, Anderson GJ, Reid DW. Pyrosequencing reveals transient cystic fibrosis lung microbiome changes with intravenous antibiotics. Eur Respir J 2014;44:922–930.