The Microbiome and Emerging Pathogens in Cystic Fibrosis and Non–Cystic Fibrosis Bronchiectasis

 

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Abstract

Chronic pulmonary sepsis is the predominant cause of morbidity for patients with cystic fibrosis (CF) and non-CF bronchiectasis. Previously it was thought that respiratory infection in these patients was mostly limited to a very small number of typical pathogens; however, in recent years there have been increasing reports of infection with other emerging potential pathogens including Burkholderia, Stenotrophomonas, Achromobacter, Ralstonia, Pandoraea, nontuberculous mycobacteria, and fungal species. Furthermore, culture-independent methodologies have established that the lungs of patients with CF and non-CF bronchiectasis comprise mixed microbiological communities of aerobic and anaerobic bacteria, fungal and viral species, collectively referred to as the lung microbiome. This article addresses the clinical relevance of emerging pathogens and the lung microbiome in CF and non-CF bronchiectasis.

• References

• 1 Burkholder WH. Sour skin, a bacterial rot of onion bulbs. Phytopathology 1950; 40: 115-118
  PubMedGoogle Scholar
• 2 Yabuuchi E, Kosako Y, Oyaizu H , et al. Proposal of Burkholderia gen. nov. and transfer of seven species of the genus Pseudomonas homology group II to the new genus, with the type species Burkholderia cepacia (Palleroni and Holmes 1981) comb. nov. Microbiol Immunol 1992; 36 (12) 1251-1275
  CrossrefPubMedGoogle Scholar
• 3 Vanlaere E, Lipuma JJ, Baldwin A , et al. Burkholderia latens sp. nov., Burkholderia diffusa sp. nov., Burkholderia arboris sp. nov., Burkholderia seminalis sp. nov. and Burkholderia metallica sp. nov., novel species within the Burkholderia cepacia complex. Int J Syst Evol Microbiol 2008; 58 (Pt 7) 1580-1590
  CrossrefPubMedGoogle Scholar
• 4 Vandamme P, Mahenthiralingam E, Holmes B , et al. Identification and population structure of Burkholderia stabilis sp. nov. (formerly Burkholderia cepacia genomovar IV). J Clin Microbiol 2000; 38 (3) 1042-1047
  PubMedGoogle Scholar
• 5 Vandamme P, Holmes B, Vancanneyt M , et al. Occurrence of multiple genomovars of Burkholderia cepacia in cystic fibrosis patients and proposal of Burkholderia multivorans sp. nov. Int J Syst Bacteriol 1997; 47 (4) 1188-1200
  CrossrefPubMedGoogle Scholar
• 6 Peeters C, Zlosnik JE, Spilker T, Hird TJ, LiPuma JJ, Vandamme P. Burkholderia pseudomultivorans sp. nov., a novel Burkholderia cepacia complex species from human respiratory samples and the rhizosphere. Syst Appl Microbiol 2013; 36 (7) 483-489
  CrossrefPubMedGoogle Scholar
• 7 Govan JR, Hughes JE, Vandamme P. Burkholderia cepacia: medical, taxonomic and ecological issues. J Med Microbiol 1996; 45 (6) 395-407
  CrossrefPubMedGoogle Scholar
• 8 Laraya-Cuasay L, Lipstein M, Huang N. Pseudomonas cepacia in the respiratory flora of patients with cystic fibrosis (CF). Pediatr Res 1977; 11: 502
  PubMedGoogle Scholar
• 9 Isles A, Maclusky I, Corey M , et al. Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J Pediatr 1984; 104 (2) 206-210
  CrossrefPubMedGoogle Scholar
• 10 Tablan OC, Chorba TL, Schidlow DV , et al. Pseudomonas cepacia colonization in patients with cystic fibrosis: risk factors and clinical outcome. J Pediatr 1985; 107 (3) 382-387
  CrossrefPubMedGoogle Scholar
• 11 Muhdi K, Edenborough FP, Gumery L , et al. Outcome for patients colonised with Burkholderia cepacia in a Birmingham adult cystic fibrosis clinic and the end of an epidemic. Thorax 1996; 51 (4) 374-377
  CrossrefPubMedGoogle Scholar
• 12 LiPuma JJ, Dasen SE, Nielson DW, Stern RC, Stull TL. Person-to-person transmission of Pseudomonas cepacia between patients with cystic fibrosis. Lancet 1990; 336 (8723) 1094-1096
  CrossrefPubMedGoogle Scholar
• 13 Govan JR, Deretic V. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia . Microbiol Rev 1996; 60 (3) 539-574
  PubMedGoogle Scholar
• 14 Govan JR, Brown PH, Maddison J , et al. Evidence for transmission of Pseudomonas cepacia by social contact in cystic fibrosis. Lancet 1993; 342 (8862) 15-19
  CrossrefPubMedGoogle Scholar
• 15 Ledson MJ, Gallagher MJ, Corkill JE, Hart CA, Walshaw MJ. Cross infection between cystic fibrosis patients colonised with Burkholderia cepacia . Thorax 1998; 53 (5) 432-436
  CrossrefPubMedGoogle Scholar
• 16 Mahenthiralingam E, Campbell ME, Henry DA, Speert DP. Epidemiology of Burkholderia cepacia infection in patients with cystic fibrosis: analysis by randomly amplified polymorphic DNA fingerprinting. J Clin Microbiol 1996; 34 (12) 2914-2920
  PubMedGoogle Scholar
• 17 Speert DP. Advances in Burkholderia cepacia complex. Paediatr Respir Rev 2002; 3 (3) 230-235
  CrossrefPubMedGoogle Scholar
• 18 Drevinek P, Mahenthiralingam E. Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin Microbiol Infect 2010; 16 (7) 821-830
  CrossrefPubMedGoogle Scholar
• 19 Coenye T, Spilker T, Van Schoor A, LiPuma JJ, Vandamme P. Recovery of Burkholderia cenocepacia strain PHDC from cystic fibrosis patients in Europe. Thorax 2004; 59 (11) 952-954
  CrossrefPubMedGoogle Scholar
• 20 Jones AM, Dodd ME, Govan JRW , et al. Burkholderia cenocepacia and Burkholderia multivorans: influence on survival in cystic fibrosis. Thorax 2004; 59 (11) 948-951
  CrossrefPubMedGoogle Scholar
• 21 Courtney JM, Dunbar KE, McDowell A , et al. Clinical outcome of Burkholderia cepacia complex infection in cystic fibrosis adults. J Cyst Fibros 2004; 3 (2) 93-98
  CrossrefPubMedGoogle Scholar
• 22 Boussaud V, Guillemain R, Grenet D , et al. Clinical outcome following lung transplantation in patients with cystic fibrosis colonised with Burkholderia cepacia complex: results from two French centres. Thorax 2008; 63 (8) 732-737
  CrossrefPubMedGoogle Scholar
• 23 Turton JF, Kaufmann ME, Mustafa N, Kawa S, Clode FE, Pitt TL. Molecular comparison of isolates of Burkholderia multivorans from patients with cystic fibrosis in the United Kingdom. J Clin Microbiol 2003; 41 (12) 5750-5754
  CrossrefPubMedGoogle Scholar
• 24 Baldwin A, Mahenthiralingam E, Drevinek P , et al. Environmental Burkholderia cepacia complex isolates in human infections. Emerg Infect Dis 2007; 13 (3) 458-461
  CrossrefPubMedGoogle Scholar
• 25 Whiteford ML, Wilkinson JD, McColl JH , et al. Outcome of Burkholderia (Pseudomonas) cepacia colonisation in children with cystic fibrosis following a hospital outbreak. Thorax 1995; 50 (11) 1194-1198
  CrossrefPubMedGoogle Scholar
• 26 Mahenthiralingam E, Coenye T, Chung JW , et al. Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J Clin Microbiol 2000; 38 (2) 910-913
  PubMedGoogle Scholar
• 27 Biddick R, Spilker T, Martin A, LiPuma JJ. Evidence of transmission of Burkholderia cepacia, Burkholderia multivorans and Burkholderia dolosa among persons with cystic fibrosis. FEMS Microbiol Lett 2003; 228 (1) 57-62
  CrossrefPubMedGoogle Scholar
• 28 Mahenthiralingam E, Vandamme P, Campbell ME , et al. Infection with Burkholderia cepacia complex genomovars in patients with cystic fibrosis: virulent transmissible strains of genomovar III can replace Burkholderia multivorans. Clin Infect Dis 2001; 33 (9) 1469-1475
  CrossrefPubMedGoogle Scholar
• 29 Silva IN, Ferreira AS, Becker JD , et al. Mucoid morphotype variation of Burkholderia multivorans during chronic cystic fibrosis lung infection is correlated with changes in metabolism, motility, biofilm formation and virulence. Microbiology 2011; 157 (Pt 11) 3124-3137
  CrossrefPubMedGoogle Scholar
• 30 Schmerk CL, Valvano MA. Burkholderia multivorans survival and trafficking within macrophages. J Med Microbiol 2013; 62 (Pt 2) 173-184
  CrossrefPubMedGoogle Scholar
• 31 Kalish LA, Waltz DA, Dovey M , et al. Impact of Burkholderia dolosa on lung function and survival in cystic fibrosis. Am J Respir Crit Care Med 2006; 173 (4) 421-425
  CrossrefPubMedGoogle Scholar
• 32 Blackburn L, Brownlee K, Conway S, Denton M. ‘Cepacia syndrome’ with Burkholderia multivorans, 9 years after initial colonization. J Cyst Fibros 2004; 3 (2) 133-134
  PubMedGoogle Scholar
• 33 Kennedy MP, Coakley RD, Donaldson SH , et al. Burkholderia gladioli: five year experience in a cystic fibrosis and lung transplantation center. J Cyst Fibros 2007; 6 (4) 267-273
  CrossrefPubMedGoogle Scholar
• 34 Murray S, Charbeneau J, Marshall BC, LiPuma JJ. Impact of burkholderia infection on lung transplantation in cystic fibrosis. Am J Respir Crit Care Med 2008; 178 (4) 363-371
  CrossrefPubMedGoogle Scholar
• 35 Church AC, Sivasothy P, Parmer J, Foweraker J. Mediastinal abscess after lung transplantation secondary to Burkholderia gladioli infection. J Heart Lung Transplant 2009; 28 (5) 511-514
  CrossrefPubMedGoogle Scholar
• 36 Quon BS, Reid JD, Wong P , et al. Burkholderia gladioli - a predictor of poor outcome in cystic fibrosis patients who receive lung transplants? A case of locally invasive rhinosinusitis and persistent bacteremia in a 36-year-old lung transplant recipient with cystic fibrosis. Can Respir J 2011; 18 (4) e64-e65
  PubMedGoogle Scholar
• 37 Brizendine K. Fatal Burkholderia gladioli infection misidentified as Empedobacter brevis in a lung transplant recipient with cystic fibrosis. Baddley, JW Pappas, PG Leon . Transpl Infect Dis 2012; 14 (4) 13-18
  CrossrefPubMedGoogle Scholar
• 38 Denton M, Kerr KG. Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia. Clin Microbiol Rev 1998; 11 (1) 57-80
  CrossrefPubMedGoogle Scholar
• 39 Blessing J, Walker J. Pseudomonas cepacia and maltophilia in the cystic-fibrosis patient. Am Rev Respir Dis 1979; 119: 262
  PubMedGoogle Scholar
• 40 Munter RG, Yinnon AM, Schlesinger Y, Hershko C. Infective endocarditis due to Stenotrophomonas (Xanthomonas) maltophilia. Eur J Clin Microbiol Infect Dis 1998; 17 (5) 353-356
  PubMedGoogle Scholar
• 41 Gopalakrishnan R, Hawley HB, Czachor JS, Markert RJ, Bernstein JM. Stenotrophomonas maltophilia infection and colonization in the intensive care units of two community hospitals: a study of 143 patients. Heart Lung 1999; 28 (2) 134-141
  CrossrefPubMedGoogle Scholar
• 42 San Gabriel P, Zhou J, Tabibi S, Chen Y, Trauzzi M, Saiman L. Antimicrobial susceptibility and synergy studies of Stenotrophomonas maltophilia isolates from patients with cystic fibrosis. Antimicrob Agents Chemother 2004; 48 (1) 168-171
  CrossrefPubMedGoogle Scholar
• 43 Cescutti P, Cuzzi B, Liut G, Segonds C, Di Bonaventura G, Rizzo R. A novel highly charged exopolysaccharide produced by two strains of Stenotrophomonas maltophilia recovered from patients with cystic fibrosis. Carbohydr Res 2011; 346 (13) 1916-1923
  CrossrefPubMedGoogle Scholar
• 44 Pompilio A, Pomponio S, Crocetta V , et al. Phenotypic and genotypic characterization of Stenotrophomonas maltophilia isolates from patients with cystic fibrosis: genome diversity, biofilm formation, and virulence. BMC Microbiol 2011; 11 (1) 159
  CrossrefPubMedGoogle Scholar
• 45 Cystic Fibrosis Foundation Patient Registry; 2010 Annual Data Report
  PubMed
• 46 Dalbøge CS, Hansen CR, Pressler T, Høiby N, Johansen HK. Chronic pulmonary infection with Stenotrophomonas maltophilia and lung function in patients with cystic fibrosis. J Cyst Fibros 2011; 10 (5) 318-325
  CrossrefPubMedGoogle Scholar
• 47 Goss CH, Otto K, Aitken ML, Rubenfeld GD. Detecting Stenotrophomonas maltophilia does not reduce survival of patients with cystic fibrosis. Am J Respir Crit Care Med 2002; 166 (3) 356-361
  CrossrefPubMedGoogle Scholar
• 48 Marchac V, Equi A, Le Bihan-Benjamin C, Hodson M, Bush A. Case-control study of Stenotrophomonas maltophilia acquisition in cystic fibrosis patients. Eur Respir J 2004; 23 (1) 98-102
  CrossrefPubMedGoogle Scholar
• 49 Waters V, Atenafu EG, Lu A, Yau Y, Tullis E, Ratjen F. Chronic Stenotrophomonas maltophilia infection and mortality or lung transplantation in cystic fibrosis patients. J Cyst Fibros 2013; 12 (5) 482-486
  CrossrefPubMedGoogle Scholar
• 50 Waters V, Yau Y, Prasad S , et al. Stenotrophomonas maltophilia in cystic fibrosis: serologic response and effect on lung disease. Am J Respir Crit Care Med 2011; 183 (5) 635-640
  CrossrefPubMedGoogle Scholar
• 51 Goss CH, Mayer-Hamblett N, Aitken ML, Rubenfeld GD, Ramsey BW. Association between Stenotrophomonas maltophilia and lung function in cystic fibrosis. Thorax 2004; 59 (11) 955-959
  CrossrefPubMedGoogle Scholar
• 52 Talmaciu I, Varlotta L, Mortensen J, Schidlow DV. Risk factors for emergence of Stenotrophomonas maltophilia in cystic fibrosis. Pediatr Pulmonol 2000; 30 (1) 10-15
  CrossrefPubMedGoogle Scholar
• 53 Krzewinski JW, Nguyen CD, Foster JM, Burns JL. Use of random amplified polymorphic DNA PCR to examine epidemiology of Stenotrophomonas maltophilia and Achromobacter (Alcaligenes) xylosoxidans from patients with cystic fibrosis. J Clin Microbiol 2001; 39 (10) 3597-3602
  CrossrefPubMedGoogle Scholar
• 54 Marzuillo C, De Giusti M, Tufi D , et al. Molecular Characterization of Stenotrophomonas maltophilia isolates from cystic fibrosis patients and the hospital environment. Infect Control Hosp Epidemiol 2009; 30 (8) 753-758
  CrossrefPubMedGoogle Scholar
• 55 Vandamme P, Moore ERB, Cnockaert M , et al. Achromobacter animicus sp. nov., Achromobacter mucicolens sp. nov., Achromobacter pulmonis sp. nov. and Achromobacter spiritinus sp. nov., from human clinical samples. Syst Appl Microbiol 2013; 36 (1) 1-10
  CrossrefPubMedGoogle Scholar
• 56 Vandamme P, Moore ERB, Cnockaert M , et al. Classification of Achromobacter genogroups 2, 5, 7 and 14 as Achromobacter insuavis sp. nov., Achromobacter aegrifaciens sp. nov., Achromobacter anxifer sp. nov. and Achromobacter dolens sp. nov., respectively. Syst Appl Microbiol 2013; 36 (7) 474-482
  CrossrefPubMedGoogle Scholar
• 57 Ridderberg W, Wang M, Nørskov-Lauritsen N. Multilocus sequence analysis of isolates of Achromobacter from patients with cystic fibrosis reveals infecting species other than Achromobacter xylosoxidans. J Clin Microbiol 2012; 50 (8) 2688-2694
  CrossrefPubMedGoogle Scholar
• 58 Spilker T, Vandamme P, Lipuma JJ. A multilocus sequence typing scheme implies population structure and reveals several putative novel Achromobacter species. J Clin Microbiol 2012; 50 (9) 3010-3015
  CrossrefPubMedGoogle Scholar
• 59 Spilker T, Vandamme P, Lipuma JJ. Identification and distribution of Achromobacter species in cystic fibrosis. J Cyst Fibros 2013; 12 (3) 298-301
  CrossrefPubMedGoogle Scholar
• 60 Cystic Fibrosis Foundation Patient Registry; 2005 Annual Data Report
  PubMed
• 61 Cystic Fibrosis Foundation Patient Registry; 2011 Annual Data Report
  PubMed
• 62 Cystic Fibrosis Foundation Patient Registry; 2012 Annual Data Report
  PubMed
• 63 De Baets F, Schelstraete P, Van Daele S, Haerynck F, Vaneechoutte M. Achromobacter xylosoxidans in cystic fibrosis: prevalence and clinical relevance. J Cyst Fibros 2007; 6 (1) 75-78
  CrossrefPubMedGoogle Scholar
• 64 Saiman L, Chen Y, Tabibi S , et al. Identification and antimicrobial susceptibility of Alcaligenes xylosoxidans isolated from patients with cystic fibrosis. J Clin Microbiol 2001; 39 (11) 3942-3945
  CrossrefPubMedGoogle Scholar
• 65 Raso T, Bianco O, Grosso B, Zucca M, Savoia D. Achromobacter xylosoxidans respiratory tract infections in cystic fibrosis patients. APMIS 2008; 116 (9) 837-841
  CrossrefPubMedGoogle Scholar
• 66 Lambiase A, Catania MR, Del Pezzo M , et al. Achromobacter xylosoxidans respiratory tract infection in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis 2011; 30 (8) 973-980
  CrossrefPubMedGoogle Scholar
• 67 Trancassini M, Iebba V, Citerà N , et al. Outbreak of Achromobacter xylosoxidans in an Italian Cystic fibrosis center: genome variability, biofilm production, antibiotic resistance, and motility in isolated strains. Front Microbiol 2014; 5 (April) 138
  PubMedGoogle Scholar
• 68 Hansen CR, Pressler T, Nielsen KG, Jensen PØ, Bjarnsholt T, Høiby N. Inflammation in Achromobacter xylosoxidans infected cystic fibrosis patients. J Cyst Fibros 2010; 9 (1) 51-58
  CrossrefPubMedGoogle Scholar
• 69 Rønne Hansen C, Pressler T, Høiby N, Gormsen M. Chronic infection with Achromobacter xylosoxidans in cystic fibrosis patients; a retrospective case control study. J Cyst Fibros 2006; 5 (4) 245-251
  CrossrefPubMedGoogle Scholar
• 70 Tan K, Conway SP, Brownlee KG, Etherington C, Peckham DG. Alcaligenes infection in cystic fibrosis. Pediatr Pulmonol 2002; 34 (2) 101-104
  CrossrefPubMedGoogle Scholar
• 71 Kanellopoulou M, Pournaras S, Iglezos H, Skarmoutsou N, Papafrangas E, Maniatis AN. Persistent colonization of nine cystic fibrosis patients with an Achromobacter (Alcaligenes) xylosoxidans clone. Eur J Clin Microbiol Infect Dis 2004; 23 (4) 336-339
  CrossrefPubMedGoogle Scholar
• 72 Van Daele S, Verhelst R, Claeys G , et al. Shared genotypes of Achromobacter xylosoxidans strains isolated from patients at a cystic fibrosis rehabilitation center. J Clin Microbiol 2005; 43 (6) 2998-3002
  CrossrefPubMedGoogle Scholar
• 73 Pereira RHV, Carvalho-Assef AP, Albano RM , et al. Achromobacter xylosoxidans: characterization of strains in Brazilian cystic fibrosis patients. J Clin Microbiol 2011; 49 (10) 3649-3651
  CrossrefPubMedGoogle Scholar
• 74 Hansen CR, Pressler T, Ridderberg W, Johansen HK, Skov M. Achromobacter species in cystic fibrosis: cross-infection caused by indirect patient-to-patient contact. J Cyst Fibros 2013; 12 (6) 609-615
  CrossrefPubMedGoogle Scholar
• 75 Dunne Jr WM, Maisch S. Epidemiological investigation of infections due to Alcaligenes species in children and patients with cystic fibrosis: use of repetitive-element-sequence polymerase chain reaction. Clin Infect Dis 1995; 20 (4) 836-841
  CrossrefPubMedGoogle Scholar
• 76 Coenye T, Falsen E, Hoste B , et al. Description of Pandoraea gen. nov. with Pandoraea apista sp. nov., Pandoraea pulmonicola sp. nov., Pandoraea pnomenusa sp. nov., Pandoraea sputorum sp. nov. and Pandoraea norimbergensis comb. nov. Int J Syst Evol Microbiol 2000; 50 (Pt 2) 887-899
  CrossrefPubMedGoogle Scholar
• 77 Pimentel JD, MacLeod C. Misidentification of Pandoraea sputorum isolated from sputum of a patient with cystic fibrosis and review of Pandoraea species infections in transplant patients. J Clin Microbiol 2008; 46 (9) 3165-3168
  CrossrefPubMedGoogle Scholar
• 78 Martínez-Lamas L, Rabade Castedo C, Martín Romero Domínguez M, Barbeito Castiñeiras G, Palacios Bartolomé A, Pérez Del Molino Bernal ML. [Pandoraea sputorum colonization in a patient with cystic fibrosis]. Arch Bronconeumol 2011; 47 (11) 571-574
  PubMedGoogle Scholar
• 79 Johnson LN, Han JY, Moskowitz SM, Burns JL, Qin X, Englund JA. Pandoraea bacteremia in a cystic fibrosis patient with associated systemic illness. Pediatr Infect Dis J 2004; 23 (9) 881-882
  CrossrefPubMedGoogle Scholar
• 80 Jørgensen 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 2003; 36 (5) 439-446
  CrossrefPubMedGoogle Scholar
• 81 Atkinson RM, Lipuma JJ, Rosenbluth DB, Dunne Jr WM. Chronic colonization with Pandoraea apista in cystic fibrosis patients determined by repetitive-element-sequence PCR. J Clin Microbiol 2006; 44 (3) 833-836
  CrossrefPubMedGoogle Scholar
• 82 Caraher E, Collins J, Herbert G , et al. Evaluation of in vitro virulence characteristics of the genus Pandoraea in lung epithelial cells. J Med Microbiol 2008; 57 (Pt 1) 15-20
  CrossrefPubMedGoogle Scholar
• 83 Costello A, Herbert G, Fabunmi L , et al. Virulence of an emerging respiratory pathogen, genus Pandoraea, in vivo and its interactions with lung epithelial cells. J Med Microbiol 2011; 60 (Pt 3) 289-299
  CrossrefPubMedGoogle Scholar
• 84 Daneshvar MI, Hollis DG, Steigerwalt AG , et al. Assignment of CDC weak oxidizer group 2 (WO-2) to the genus Pandoraea and characterization of three new Pandoraea genomospecies. J Clin Microbiol 2001; 39 (5) 1819-1826
  CrossrefPubMedGoogle Scholar
• 85 Stryjewski ME, LiPuma JJ, Messier Jr RH, Reller LB, Alexander BD. Sepsis, multiple organ failure, and death due to Pandoraea pnomenusa infection after lung transplantation. J Clin Microbiol 2003; 41 (5) 2255-2257
  CrossrefPubMedGoogle Scholar
• 86 Yabuuchi E, Kosako Y, Yano I, Hotta H, Nishiuchi Y. Transfer of two Burkholderia and an Alcaligenes species to Ralstonia gen. Nov.: Proposal of Ralstonia pickettii (Ralston, Palleroni and Doudoroff 1973) comb. Nov., Ralstonia solanacearum (Smith 1896) comb. Nov. and Ralstonia eutropha (Davis 1969) comb. Nov. Microbiol Immunol 1995; 39 (11) 897-904
  CrossrefPubMedGoogle Scholar
• 87 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 2002; 8 (7) 692-696
  CrossrefPubMedGoogle Scholar
• 88 Coenye T, Spilker T, Reik R, Vandamme P, Lipuma JJ. Use of PCR analyses to define the distribution of Ralstonia species recovered from patients with cystic fibrosis. J Clin Microbiol 2005; 43 (7) 3463-3466
  CrossrefPubMedGoogle Scholar
• 89 Daxboeck F, Stadler M, Assadian O, Marko E, Hirschl AM, Koller W. Characterization of clinically isolated Ralstonia mannitolilytica strains using random amplification of polymorphic DNA (RAPD) typing and antimicrobial sensitivity, and comparison of the classification efficacy of phenotypic and genotypic assays. J Med Microbiol 2005; 54 (Pt 1) 55-61
  CrossrefPubMedGoogle Scholar
• 90 Lipuma JJ. The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev 2010; 23 (2) 299-323
  CrossrefPubMedGoogle Scholar
• 91 Burns JL, Emerson J, Stapp JR , et al. Microbiology of sputum from patients at cystic fibrosis centers in the United States. Clin Infect Dis 1998; 27 (1) 158-163
  CrossrefPubMedGoogle Scholar
• 92 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 (9) 995-1001
  CrossrefPubMedGoogle Scholar
• 93 Worlitzsch D, Rintelen C, Böhm K , et al. Antibiotic-resistant obligate anaerobes during exacerbations of cystic fibrosis patients. Clin Microbiol Infect 2009; 15 (5) 454-460
  CrossrefPubMedGoogle Scholar
• 94 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 2008; 43 (5) 490-497
  CrossrefPubMedGoogle Scholar
• 95 Field TR, Sibley CD, Parkins MD, Rabin HR, Surette MG. The genus Prevotella in cystic fibrosis airways. Anaerobe 2010; 16 (4) 337-344
  CrossrefPubMedGoogle Scholar
• 96 Ulrich M, Beer I, Braitmaier P , et al. Relative contribution of Prevotella intermedia and Pseudomonas aeruginosa to lung pathology in airways of patients with cystic fibrosis. Thorax 2010; 65 (11) 978-984
  CrossrefPubMedGoogle Scholar
• 97 Duan K, Dammel C, Stein J, Rabin H, Surette MG. Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol Microbiol 2003; 50 (5) 1477-1491
  CrossrefPubMedGoogle Scholar
• 98 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 (7) 579-584
  CrossrefPubMedGoogle Scholar
• 99 Zemanick ET, Harris JK, Wagner BD , et al. Inflammation and airway microbiota during cystic fibrosis pulmonary exacerbations. PLoS ONE 2013; 8 (4) e62917
  CrossrefPubMedGoogle Scholar
• 100 Tunney MM, Einarsson GG, Wei L , et al. Lung microbiota and bacterial abundance in patients with bronchiectasis when clinically stable and during exacerbation. Am J Respir Crit Care Med 2013; 187 (10) 1118-1126
  CrossrefPubMedGoogle Scholar
• 101 Zhao J, Schloss PD, Kalikin LM , et al. Decade-long bacterial community dynamics in cystic fibrosis airways. Proc Natl Acad Sci U S A 2012; 109 (15) 5809-5814
  CrossrefPubMedGoogle Scholar
• 102 Bittar F, Richet H, Dubus J-C , et al. Molecular detection of multiple emerging pathogens in sputa from cystic fibrosis patients. PLoS ONE 2008; 3 (8) e2908
  CrossrefPubMedGoogle Scholar
• 103 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 2004; 42 (11) 5176-5183
  CrossrefPubMedGoogle Scholar
• 104 Cox MJ, Allgaier M, Taylor B , et al. Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PLoS ONE 2010; 5 (6) e11044
  CrossrefPubMedGoogle Scholar
• 105 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 (9) e45001
  CrossrefPubMedGoogle Scholar
• 106 UK Cystic Fibrosis Registry Annual Data Report; 2012
  PubMed