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

Expert Review of Respiratory Medicine

Volumn 5, Issue 6, 2011, Pages 809-821

  Huang, Yvonne J ^a   Lynch, Susan V ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

16S ribosomal RNA; Asthma; COPD; Cystic fibrosis; Microbiota; Next generation Sequencing; PhyloChip

Indexed keywords

TOBRAMYCIN;

ASTHMA; CELL CULTURE; CHLAMYDOPHILA PNEUMONIAE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CHRONIC RESPIRATORY TRACT DISEASE; CYSTIC FIBROSIS; HAEMOPHILUS INFLUENZAE; HUMAN; LOWER RESPIRATORY TRACT; MICROBIAL BIOMASS; MICROBIAL COMMUNITY; MORAXELLA CATARRHALIS; MYCOPLASMA PNEUMONIAE; PSEUDOMONAS AERUGINOSA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; STREPTOCOCCUS PNEUMONIAE; UPPER RESPIRATORY TRACT INFECTION;

EID: 81255157031     PISSN: 17476348     EISSN: 17476356     Source Type: Journal    
DOI: 10.1586/ers.11.76     Document Type: Review

References (108)

1. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444(7122), 1027-1031 (2006). (Pubitemid 46018515)
2. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature 444(7122), 1022-1023 (2006). (Pubitemid 46018512)
3. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc. Natl Acad. Sci. USA 102(31), 11070-11075 (2005). (Pubitemid 41105994)
4. 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).
5. 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). (Pubitemid 43066642)
6. Hahn DL, Dodge RW, Golubjatnikov R. Association of Chlamydia pneumoniae (strain TWAR) infection with wheezing, asthmatic bronchitis, and adult-onset asthma. JAMA 266(2), 225-230 (1991).
7. 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. Infection 31(5), 367-368 (2003). (Pubitemid 37260377)
8. 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). (Pubitemid 24147080)
9. 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. Respirology 9(2), 255-259 (2004). (Pubitemid 38937401)
10. 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 Pt1), 391-392 (2000). (Pubitemid 30109057)
11. 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). (Pubitemid 32210024)
12. Kocabas A, Avsar M, Hanta I, Koksal F, Kuleci S. Chlamydophila pneumoniae infection in adult asthmatics patients. J. Asthma 45(1), 39-43 (2008). (Pubitemid 351225441)
13. 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). (Pubitemid 32397743)
14. Specjalski K, Jassem E. Chlamydophila pneumoniae, Mycoplasma pneumoniae infections, and asthma control. Allergy Asthma Proc. 32(2), 9-17 (2011).
15. 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). (Pubitemid 47572634)
16. Bisgaard H, Hermansen MN, Bonnelykke K et al. Association of bacteria and viruses with wheezy episodes in young children: prospective birth cohort study. BMJ 341, c4978 (2010).
17. 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).
18. 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). (Pubitemid 36143293)
19. 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). (Pubitemid 46654175)
20. 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 65(12), 1045-1052 (2010).
21. Sigurs N. A cohort of children hospitalised with acute RSV bronchiolitis: impact on later respiratory disease. Paediatr. Respir. Rev. 3(3), 177-183 (2002). (Pubitemid 35314878)
22. 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). (Pubitemid 40105412)
23. Dulek DE, Peebles RS Jr. Viruses and asthma. Biochim. Biophys. Acta doi:10. 1016/j. bbagen. 2011. 01. 012 (2011) (Epub ahead of print).
24. 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). (Pubitemid 46700945)
25. 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). (Pubitemid 351600663)
26. 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). (Pubitemid 40981193)
27. 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). (Pubitemid 43726892)
28. 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). (Pubitemid 34879333)
29. 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). (Pubitemid 351442187)
30. Sethi S, Murphy TF. Infection in the pathogenesis and course of chronic obstructive pulmonary disease. N. Engl. J. Med. 359(22), 2355-2365 (2008).
31. 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).
32. 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).
33. 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).
34. 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).
35. Kherad O, Kaiser L, Bridevaux PO et al. Upper-respiratory viral infection, biomarkers, and COPD exacerbations. Chest 138(4), 896-904 (2010).
36. 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. Chest 129(2), 317-324 (2006). (Pubitemid 43289850)
37. Avadhanula V, Rodriguez CA, Devincenzo JP et al. Respiratory viruses augment the adhesion of bacterial pathogens to respiratory epithelium in a viral speciesand cell type-dependent manner. J. Virol. 80(4), 1629-1636 (2006). (Pubitemid 43228704)
38. 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).
39. 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).
40. 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). (Pubitemid 40563235)
41. 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).
42. 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).
43. 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).
44. Morris A, Sciurba FC, Norris KA. Pneumocystis: a novel pathogen in chronic obstructive pulmonary disease?. COPD 5(1), 43-51 (2008). (Pubitemid 351225519)
45. 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). (Pubitemid 32778218)
46. 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). (Pubitemid 37266030)
47. 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). (Pubitemid 34764734)
48. 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).
49. 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). (Pubitemid 37296706)
50. 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).
51. 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). (Pubitemid 351657317)
52. Canton R, Morosini MI, Ballestero S et al. Lung colonization with Enterobacteriaceae producing extended-spectrum b-lactamases in cystic fibrosis patients. Pediatr. Pulmonol. 24(3), 213-217 (1997). (Pubitemid 27431231)
53. 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).
54. 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).
55. 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).
56. 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).
57. Bik EM, Eckburg PB, Gill SR et al. Molecular analysis of the bacterial microbiota in the human stomach. Proc. Natl Acad. Sci. USA 103(3), 732-737 (2006). (Pubitemid 43153094)
58. Dewhirst FE, Chen T, Izard J et al. The human oral microbiome. J. Bacteriol. 192(19), 5002-5017 (2010).
59. Eckburg PB, Bik EM, Bernstein CN et al. Diversity of the human intestinal microbial flora. Science 308(5728), 1635-1638 (2005). (Pubitemid 40807514)
60. Grice EA, Segre JA. The skin microbiome. Nat. Rev. Microbiol. 9(4), 244-253 (2011).
61. Brodie EL, Desantis TZ, Parker JP, Zubietta IX, Piceno YM, Andersen GL. Urban aerosols harbor diverse and dynamic bacterial populations. Proc. Natl Acad. Sci. USA 104(1), 299-304 (2007). (Pubitemid 46068026)
62. 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). (Pubitemid 46716624)
63. Lemos LN, Fulthorpe RR, Triplett EW, Roesch LF. Rethinking microbial diversity analysis in the high throughput sequencing era. J. Microbiol. Methods 86(1), 42-51 (2011).
64. Petrosino JF, Highlander S, Luna RA, Gibbs RA, Versalovic J. Metagenomic pyrosequencing and microbial identification. Clin. Chem. 55(5), 856-866 (2009).
65. 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).
66. Ghannoum MA, Jurevic RJ, Mukherjee PK et al. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog. 6(1), e1000713 (2010).
67. 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). (Pubitemid 47378930)
68. 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). (Pubitemid 44228592)
69. Wang D, Coscoy L, Zylberberg M et al. Microarray-based detection and genotyping of viral pathogens. Proc. Natl Acad. Sci. USA 99(24), 15687-15692 (2002). (Pubitemid 35403992)
70. Reyes A, Haynes M, Hanson N et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466(7304), 334-338 (2010).
71. Dethlefsen L, Mcfall-Ngai M, Relman DA. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449(7164), 811-818 (2007). (Pubitemid 47598621)
72. 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).
73. 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).
74. 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. MBio 1(3) e00129-10 (2010).
75. Zaura E, Keijser BJ, Huse SM, Crielaard W. Defining the healthy core microbiome' of oral microbial communities. BMC Microbiol. 9, 259 (2009).
76. Arumugam M, Raes J, Pelletier E et al. Enterotypes of the human gut microbiome. Nature 473(7346), 174-180 (2011).
77. Norris KA, Morris A. Pneumocystis infection and the pathogenesis of chronic obstructive pulmonary disease. Immunol. Res. 50(2-3), 175-180 (2011).
78. 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).
79. 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).
80. Muller FM, Seidler M. Characteristics of pathogenic fungi and antifungal therapy in cystic fibrosis. Expert Rev. Anti Infect. Ther. 8(8), 957-964 (2010).
81. 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).
82. 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).
83. Hilty M, Burke C, Pedro H et al. Disordered microbial communities in asthmatic airways. PLoS One 5(1), e8578 (2010).
84. Charlson ES, Chen J, Custers-Allen R et al. Disordered microbial communities in the upper respiratory tract of cigarette smokers. PLoS One 5(12), e15216 (2010).
85. 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). (Pubitemid 39587496)
86. Ichinohe T, Pang IK, Kumamoto Y et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl Acad. Sci. USA 108(13), 5354-5359 (2011).
87. Erb-Downward JR, Thompson DL, Han MK et al. Analysis of the lung microbiome in the healthy' smoker and in COPD. PLoS One 6(2), e16384 (2011).
88. Huang YJ, Kim E, Cox MJ et al. A persistent and diverse airway microbiota present during chronic obstructive pulmonary disease exacerbations. OMICS 14(1), 9-59 (2010).
89. Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 8(6), 411-420 (2008). (Pubitemid 351733416)
90. 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). (Pubitemid 36994681)
91. Rogers GB, Carroll MP, Serisier DJ et al. Bacterial activity in cystic fibrosis lung infections. Respir. Res. 6, 49 (2005).
92. 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). (Pubitemid 39506227)
93. 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. USA 104(51), 20529-20533 (2007).
94. 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).
95. Cox MJ, Allgaier M, Taylor B et al. Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PLoS One 5(6), e11044 (2010).
96. 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). (Pubitemid 38010446)
97. 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).
98. Høiby N, Ciofu O, Johansen HK et al. The clinical impact of bacterial biofilms. Int. J. Oral Sci. 3(2), 55-65 (2011).
99. Campos J, Roman F, Georgiou M et al. Long-term persistence of ciprofloxacinresistant Haemophilus influenzae in patients with cystic fibrosis. J. Infect. Dis. 174(6), 1345-1347 (1996). (Pubitemid 26393919)
100. 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).
101. 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). (Pubitemid 29326116)
102. 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). (Pubitemid 43176597)
103. Drevinek P, Mahenthiralingam E. Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin. Microbiol. Infect. 16(7), 821-830 (2010).
104. 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). (Pubitemid 37267172)
105. 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).
106. 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).
107. Bauernfeind A, Bertele RM, Harms K et al. Qualitative and quantitative microbiological analysis of sputa of 102 patients with cystic fibrosis. Infection 15(4), 270-277 (1987).
108. 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). (Pubitemid 40656228)