Emerging bacterial pathogens and changing concepts of bacterial pathogenesis in cystic fibrosis

Journal of Cystic Fibrosis

Volumn 14, Issue 3, 2015, Pages 293-304

  Parkins, Michael D ^a,b   Floto, R Andres ^c,d  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d PAPWORTH HOSPITAL   (United Kingdom)

Author keywords

Achromobacter xylosoxidans; Methicillin resistant Staphylococcus aureus (MRSA); Microbiome; Mycobacterium abscessus; Mycobacterium avium complex; Stenotrophomonas maltophilia

Indexed keywords

ACHROMOBACTER; ACHROMOBACTER XYLOSOXIDANS; AGING; ATYPICAL MYCOBACTERIUM; BACTERIUM IDENTIFICATION; BURKHOLDERIA CEPACIA COMPLEX; CLINICAL FEATURE; DISEASE COURSE; HUMAN; INFECTION RISK; LOWER RESPIRATORY TRACT INFECTION; LUNG FIBROSIS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MORBIDITY; MORTALITY; PATHOGENESIS; PSEUDOMONAS AERUGINOSA; REVIEW; SPUTUM ANALYSIS; STAPHYLOCOCCUS AUREUS; STENOTROPHOMONAS MALTOPHILIA; BACTERIUM; CYSTIC FIBROSIS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MICROFLORA; SPUTUM;

BACTERIA; CYSTIC FIBROSIS; HUMANS; MICROBIOTA; SPUTUM;

EID: 84937517061     PISSN: 15691993     EISSN: 18735010     Source Type: Journal    
DOI: 10.1016/j.jcf.2015.03.012     Document Type: Review

References (131)

1. Millar F.A., Simmonds N.J., Hodson M.E. Trends in pathogens colonising the respiratory tract of adult patients with cystic fibrosis, 1985-2005. J Cyst Fibros Dec 2009, 8(6):386-391.
2. Emerson J., McNamara S., Buccat A.M., Worrell K., Burns J.L. Changes in cystic fibrosis sputum microbiology in the United States between 1995 and 2008. Pediatr Pulmonol Apr 2010, 45(4):363-370.
3. Lipuma J.J. The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev Apr 2010, 23(2):299-323.
4. Ingram R. CF matters [cited 2014 Sept, 14]; Available from:. http://www.cfmatters.ue.
5. Cole J.R., Wang Q., Cardenas E., Fish J., Chai B., Farris R.J., et al. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res Jan 2009, 37:D141-D145. [Database issue].
6. Fernandez-Olmos A., Garcia-Castillo M., Morosini M.I., Lamas A., Maiz L., Canton R. MALDI-TOF MS improves routine identification of non-fermenting Gram negative isolates from cystic fibrosis patients. J Cyst Fibros Jan 2012, 11(1):59-62.
7. Marko D.C., Saffert R.T., Cunningham S.A., Hyman J., Walsh J., Arbefeville S., et al. Evaluation of the Bruker Biotyper and Vitek MS matrix-assisted laser desorption ionization-time of flight mass spectrometry systems for identification of nonfermenting Gram-negative bacilli isolated from cultures from cystic fibrosis patients. J Clin Microbiol Jun 2012, 50(6):2034-2039.
8. Enright M.C., Robinson D.A., Randle G., Feil E.J., Grundmann H., Spratt B.G. The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci U S A May 28 2002, 99(11):7687-7692.
9. Moran G.J., Krishnadasan A., Gorwitz R.J., Fosheim G.E., McDougal L.K., Carey R.B., et al. Methicillin-resistant S. aureus infections among patients in the emergency department. N Engl J Med Aug 17 2006, 355(7):666-674.
10. Dasenbrook E.C. Update on methicillin-resistant Staphylococcus aureus in cystic fibrosis. Curr Opin Pulm Med Nov 2011, 17(6):437-441.
11. Champion E.A., Miller M.B., Popowitch E.B., Hobbs M.M., Saiman L., Muhlebach M.S., et al. Antimicrobial susceptibility and molecular typing of MRSA in cystic fibrosis. Pediatr Pulmonol Mar 2014, 49(3):230-237.
12. Glikman D., Siegel J.D., David M.Z., Okoro N.M., Boyle-Vavra S., Dowell M.L., et al. Complex molecular epidemiology of methicillin-resistant Staphylococcus aureus isolates from children with cystic fibrosis in the era of epidemic community-associated methicillin-resistant S aureus. Chest Jun 2008, 133(6):1381-1387.
13. Zuckerman J.B., Zuaro D.E., Prato B.S., Ruoff K.L., Sawicki R.W., Quinton H.B., et al. Bacterial contamination of cystic fibrosis clinics. J Cyst Fibros May 2009, 8(3):186-192.
14. Nadesalingam K., Conway S.P., Denton M. Risk factors for acquisition of methicillin-resistant Staphylococcus aureus (MRSA) by patients with cystic fibrosis. J Cyst Fibros Mar 2005, 4(1):49-52.
15. Stone A., Quittell L., Zhou J., Alba L., Bhat M., DeCelie-Germana J., et al. Staphylococcus aureus nasal colonization among pediatric cystic fibrosis patients and their household contacts. Pediatr Infect Dis J Oct 2009, 28(10):895-899.
16. Fritz S.A., Hogan P.G., Singh L.N., Thompson R.M., Wallace M.A., Whitney K., et al. Contamination of environmental surfaces with Staphylococcus aureus in households with children infected with methicillin-resistant S. aureus. JAMA Pediatr Nov 1 2014, 168(11):1030-1038.
17. Ren C.L., Morgan W.J., Konstan M.W., Schechter M.S., Wagener J.S., Fisher K.A., et al. Presence of methicillin resistant Staphylococcus aureus in respiratory cultures from cystic fibrosis patients is associated with lower lung function. Pediatr Pulmonol Jun 2007, 42(6):513-518.
18. Dasenbrook E.C., Merlo C.A., Diener-West M., Lechtzin N., Boyle M.P. Persistent methicillin-resistant Staphylococcus aureus and rate of FEV1 decline in cystic fibrosis. Am J Respir Crit Care Med Oct 15 2008, 178(8):814-821.
19. Sanders D.B., Bittner R.C., Rosenfeld M., Hoffman L.R., Redding G.J., Goss C.H. Failure to recover to baseline pulmonary function after cystic fibrosis pulmonary exacerbation. Am J Respir Crit Care Med Sep 1 2010, 182(5):627-632.
20. Dasenbrook E.C., Checkley W., Merlo C.A., Konstan M.W., Lechtzin N., Boyle M.P. Association between respiratory tract methicillin-resistant Staphylococcus aureus and survival in cystic fibrosis. JAMA Jun 16 2010, 303(23):2386-2392.
21. Liu G.Y. Molecular pathogenesis of Staphylococcus aureus infection. Pediatr Res May 2009, 65(5 Pt 2):71R-77R.
22. Powers M.E., Bubeck Wardenburg J. Igniting the fire: Staphylococcus aureus virulence factors in the pathogenesis of sepsis. PLoS Pathog Feb 2014, 10(2):e1003871.
23. Al-Zubeidi D., Hogan P.G., Boyle M., Burnham C.A., Fritz S.A. Molecular epidemiology of methicillin-resistant Staphylococcus aureus isolated in serial cultures from the respiratory tract of children with cystic fibrosis. Pediatr Infect Dis J Jun 2014, 33(6):549-553.
24. Filleron A., Chiron R., Reverdy M.E., Jean-Pierre H., Dumitrescu O., Aleyrangues L., et al. Staphylococcus aureus with decreased susceptibility to glycopeptides in cystic fibrosis patients. J Cyst Fibros Sep 2011, 10(5):377-382.
25. Cafiso V., Bertuccio T., Spina D., Campanile F., Bongiorno D., Santagati M., et al. Methicillin resistance and vancomycin heteroresistance in Staphylococcus aureus in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis Oct 2010, 29(10):1277-1285.
26. Hill R.L., Kearns A.M., Nash J., North S.E., Pike R., Newson T., et al. Linezolid-resistant ST36 methicillin-resistant Staphylococcus aureus associated with prolonged linezolid treatment in two paediatric cystic fibrosis patients. J Antimicrob Chemother Mar 2010, 65(3):442-445.
27. Long S.W., Olsen R.J., Mehta S.C., Palzkill T., Cernoch P.L., Perez K.K., et al. PBP2a mutations causing high-level ceftaroline resistance in clinical methicillin-resistant Staphylococcus aureus isolates. Antimicrob Agents Chemother Nov 2014, 58(11):6668-6674.
28. Parkins M.D., Elborn J.S. Newer antibacterial agents and their potential role in cystic fibrosis pulmonary exacerbation management. J Antimicrob Chemother Sep 2010, 65(9):1853-1861.
29. Sawicki G.S., Rasouliyan L., Pasta D.J., Regelmann W.E., Wagener J.S., Waltz D.A., et al. The impact of incident methicillin resistant Staphylococcus aureus detection on pulmonary function in cystic fibrosis. Pediatr Pulmonol Nov 2008, 43(11):1117-1123.
30. Trust C.F. Antibiotic treatment for cystic fibrosis 2009, 1-102. UK CF Trust, Bromley, Kent UK.
31. Lamer C., de Beco V., Soler P., Calvat S., Fagon J.Y., Dombret M.C., et al. Analysis of vancomycin entry into pulmonary lining fluid by bronchoalveolar lavage in critically ill patients. Antimicrob Agents Chemother Feb 1993, 37(2):281-286.
32. Wunderink R.G., Niederman M.S., Kollef M.H., Shorr A.F., Kunkel M.J., Baruch A., et al. Linezolid in methicillin-resistant Staphylococcus aureus nosocomial pneumonia: a randomized, controlled study. Clin Infect Dis Mar 1 2012, 54(5):621-629.
33. Sexton P., Harrison A.C. Susceptibility to nontuberculous mycobacterial lung disease. Eur Respir J Jun 2008, 31(6):1322-1333.
34. Kim R.D., Greenberg D.E., Ehrmantraut M.E., Guide S.V., Ding L., Shea Y., et al. Pulmonary nontuberculous mycobacterial disease: prospective study of a distinct preexisting syndrome. Am J Respir Crit Care Med Nov 15 2008, 178(10):1066-1074.
35. Ziedalski T.M., Kao P.N., Henig N.R., Jacobs S.S., Ruoss S.J. Prospective analysis of cystic fibrosis transmembrane regulator mutations in adults with bronchiectasis or pulmonary nontuberculous mycobacterial infection. Chest Oct 2006, 130(4):995-1002.
36. Griffith D.E., Aksamit T., Brown-Elliott B.A., Catanzaro A., Daley C., Gordin F., et al. An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med Feb 15 2007, 175(4):367-416.
37. Roux A.L., Catherinot E., Ripoll F., Soismier N., Macheras E., Ravilly S., et al. Multicenter study of prevalence of nontuberculous mycobacteria in patients with cystic fibrosis in France. J Clin Microbiol Dec 2009, 47(12):4124-4128.
38. Esther C.R., Esserman D.A., Gilligan P., Kerr A., Noone P.G. Chronic Mycobacterium abscessus infection and lung function decline in cystic fibrosis. J Cyst Fibros Mar 2010, 9(2):117-123.
39. Rodman D.M., Polis J.M., Heltshe S.L., Sontag M.K., Chacon C., Rodman R.V., et al. Late diagnosis defines a unique population of long-term survivors of cystic fibrosis. Am J Respir Crit Care Med Mar 15 2005, 171(6):621-626. [Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.].
40. Levy I., Grisaru-Soen G., Lerner-Geva L., Kerem E., Blau H., Bentur L., et al. Multicenter cross-sectional study of nontuberculous mycobacterial infections among cystic fibrosis patients, Israel. Emerg Infect Dis Mar 2008, 14(3):378-384.
41. Bar-On O., Mussaffi H., Mei-Zahav M., Prais D., Steuer G., Stafler P., et al. Increasing nontuberculous mycobacteria infection in cystic fibrosis. J Cyst Fibros Jun 2014, 7.
42. Catherinot E., Roux A.L., Vibet M.A., Bellis G., Ravilly S., Lemonnier L., et al. Mycobacterium avium and Mycobacterium abscessus complex target distinct cystic fibrosis patient subpopulations. J Cyst Fibros Jan 2013, 12(1):74-80.
43. Renna M., Schaffner C., Brown K., Shang S., Tamayo M.H., Hegyi K., et al. Azithromycin blocks autophagy and may predispose cystic fibrosis patients to mycobacterial infection. J Clin Invest Sep 2011, 121(9):3554-3563. [Research Support, Non-U.S. Gov't].
44. Aitken M.L., Limaye A., Pottinger P., Whimbey E., Goss C.H., Tonelli M.R., et al. Respiratory outbreak of Mycobacterium abscessus subspecies massiliense in a lung transplant and cystic fibrosis center. Am J Respir Crit Care Med Jan 15 2012, 185(2):231-232. [Letter].
45. Bryant J.M., Grogono D.M., Parkhill J., Floto R.A. Transmission of M. abscessus in patients with cystic fibrosis - authors' reply. Lancet Aug 10 2013, 382(9891):504. [Comment Letter].
46. Adekambi T., Berger P., Raoult D., Drancourt M. rpoB gene sequence-based characterization of emerging non-tuberculous mycobacteria with descriptions of Mycobacterium bolletii sp. nov., Mycobacterium phocaicum sp. nov. and Mycobacterium aubagnense sp. nov. Int J Syst Evol Microbiol Jan 2006, 56(Pt 1):133-143.
47. Bange F.C., Kirschner P., Bottger E.C. Recovery of mycobacteria from patients with cystic fibrosis. J Clin Microbiol Nov 1999, 37(11):3761-3763.
48. Adekambi T., Reynaud-Gaubert M., Greub G., Gevaudan M.J., La Scola B., Raoult D., et al. Amoebal coculture of "Mycobacterium massiliense" sp. nov. from the sputum of a patient with hemoptoic pneumonia. J Clin Microbiol Dec 2004, 42(12):5493-5501. [Case Reports].
49. Olivier K.N., Weber D.J., Wallace R.J., Faiz A.R., Lee J.H., Zhang Y., et al. Nontuberculous mycobacteria. I: multicenter prevalence study in cystic fibrosis. Am J Respir Crit Care Med Mar 15 2003, 167(6):828-834.
50. Chernenko S.M., Humar A., Hutcheon M., Chow C.W., Chaparro C., Keshavjee S., et al. Mycobacterium abscessus infections in lung transplant recipients: the international experience. J Heart Lung Transplant Dec 2006, 25(12):1447-1455.
51. Amoureux L., Bador J., Fardeheb S., Mabille C., Couchot C., Massip C., et al. Detection of Achromobacter xylosoxidans in hospital, domestic, and outdoor environmental samples and comparison with human clinical isolates. Appl Environ Microbiol Dec 2013, 79(23):7142-7149.
52. Spilker T., Vandamme P., Lipuma J.J. Identification and distribution of Achromobacter species in cystic fibrosis. J Cyst Fibros May 2013, 12(3):298-301.
53. Raso T., Bianco O., Grosso B., Zucca M., Savoia D. Achromobacter xylosoxidans respiratory tract infections in cystic fibrosis patients. APMIS Sep 2008, 116(9):837-841.
54. Spicuzza L., Sciuto C., Vitaliti G., Di Dio G., Leonardi S., La Rosa M. Emerging pathogens in cystic fibrosis: ten years of follow-up in a cohort of patients. Eur J Clin Microbiol Infect Dis Feb 2009, 28(2):191-195.
55. De Baets F., Schelstraete P., Van Daele S., Haerynck F., Vaneechoutte M. Achromobacter xylosoxidans in cystic fibrosis: prevalence and clinical relevance. J Cyst Fibros Jan 2007, 6(1):75-78.
56. Saiman L., Chen Y., Tabibi S., San Gabriel P., Zhou J., Liu Z., et al. Identification and antimicrobial susceptibility of Alcaligenes xylosoxidans isolated from patients with cystic fibrosis. J Clin Microbiol Nov 2001, 39(11):3942-3945.
57. Lambiase A., Catania M.R., Del Pezzo M., Rossano F., Terlizzi V., Sepe A., et al. Achromobacter xylosoxidans respiratory tract infection in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis Aug 2011, 30(8):973-980.
58. Ridderberg W., Bendstrup K.E., Olesen H.V., Jensen-Fangel S., Norskov-Lauritsen N. Marked increase in incidence of Achromobacter xylosoxidans infections caused by sporadic acquisition from the environment. J Cyst Fibros Dec 2011, 10(6):466-469.
59. Ronne Hansen C., Pressler T., Hoiby N., Gormsen M. Chronic infection with Achromobacter xylosoxidans in cystic fibrosis patients; a retrospective case control study. J Cyst Fibros Dec 2006, 5(4):245-251.
60. Caillon J.L.V., Carrere J., Pelletier M., Batard E., Jacqueline C. [Abstract E-1469] In vitro activity of meropenem (MEM), colistin (CS) and tigecycline (TGC) against Achromobacter xylosoxidans (AX) Isolated from cystic fibrosis patients. 49th Interscience Conference on Antimicrobial Agents and Chemotherapy 2009.
61. Hanes S.D., Demirkan K., Tolley E., Boucher B.A., Croce M.A., Wood G.C., et al. Risk factors for late-onset nosocomial pneumonia caused by Stenotrophomonas maltophilia in critically ill trauma patients. Clin Infect Dis Aug 1 2002, 35(3):228-235.
62. Tseng C.C., Fang W.F., Huang K.T., Chang P.W., Tu M.L., Shiang Y.P., et al. Risk factors for mortality in patients with nosocomial Stenotrophomonas maltophilia pneumonia. Infect Control Hosp Epidemiol Dec 2009, 30(12):1193-1202.
63. Brooke J.S. New strategies against Stenotrophomonas maltophilia: a serious worldwide intrinsically drug-resistant opportunistic pathogen. Expert Rev Anti Infect Ther Jan 2014, 12(1):1-4.
64. Brooke J.S. Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clin Microbiol Rev Jan 2012, 25(1):2-41.
65. Vidigal P.G., Dittmer S., Steinmann E., Buer J., Rath P.M., Steinmann J. Adaptation of Stenotrophomonas maltophilia in cystic fibrosis: molecular diversity, mutation frequency and antibiotic resistance. Int J Med Microbiol Jul 2014, 304(5-6):613-619.
66. Ballestero S., Virseda I., Escobar H., Suarez L., Baquero F. Stenotrophomonas maltophilia in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis Aug 1995, 14(8):728-729.
67. Graff G.R., Burns J.L. Factors affecting the incidence of Stenotrophomonas maltophilia isolation in cystic fibrosis. Chest Jun 2002, 121(6):1754-1760.
68. Goss C.H., Mayer-Hamblett N., Aitken M.L., Rubenfeld G.D., Ramsey B.W. Association between Stenotrophomonas maltophilia and lung function in cystic fibrosis. Thorax Nov 2004, 59(11):955-959.
69. Stanojevic S., Ratjen F., Stephens D., Lu A., Yau Y., Tullis E., et al. Factors influencing the acquisition of Stenotrophomonas maltophilia infection in cystic fibrosis patients. J Cyst Fibros Dec 2013, 12(6):575-583.
70. Denton M., Todd N.J., Littlewood J.M. Role of anti-pseudomonal antibiotics in the emergence of Stenotrophomonas maltophilia in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis May 1996, 15(5):402-405.
71. Burns J.L., Van Dalfsen J.M., Shawar R.M., Otto K.L., Garber R.L., Quan J.M., et al. Effect of chronic intermittent administration of inhaled tobramycin on respiratory microbial flora in patients with cystic fibrosis. J Infect Dis May 1999, 179(5):1190-1196.
72. Goss C.H., Otto K., Aitken M.L., Rubenfeld G.D. Detecting Stenotrophomonas maltophilia does not reduce survival of patients with cystic fibrosis. Am J Respir Crit Care Med Aug 1 2002, 166(3):356-361.
73. Waters V., Yau Y., Prasad S., Lu A., Atenafu E., Crandall I., et al. Stenotrophomonas maltophilia in cystic fibrosis: serologic response and effect on lung disease. Am J Respir Crit Care Med Mar 1 2011, 183(5):635-640.
74. Waters V., Atenafu E.G., Salazar J.G., Lu A., Yau Y., Matukas L., et al. Chronic Stenotrophomonas maltophilia infection and exacerbation outcomes in cystic fibrosis. J Cyst Fibros Jan 2012, 11(1):8-13.
75. Waters V., Atenafu E.G., Lu A., Yau Y., Tullis E., Ratjen F. Chronic Stenotrophomonas maltophilia infection and mortality or lung transplantation in cystic fibrosis patients. J Cyst Fibros Sep 2013, 12(5):482-486.
76. Canton R., Valdezate S., Vindel A., Sanchez Del Saz B., Maiz L., Baquero F. Antimicrobial susceptibility profile of molecular typed cystic fibrosis Stenotrophomonas maltophilia isolates and differences with noncystic fibrosis isolates. Pediatr Pulmonol Feb 2003, 35(2):99-107.
77. Valenza G., Tappe D., Turnwald D., Frosch M., Konig C., Hebestreit H., et al. Prevalence and antimicrobial susceptibility of microorganisms isolated from sputa of patients with cystic fibrosis. J Cyst Fibros Mar 2008, 7(2):123-127.
78. Goncalves-Vidigal P., Grosse-Onnebrink J., Mellies U., Buer J., Rath P.M., Steinmann J. Stenotrophomonas maltophilia in cystic fibrosis: improved detection by the use of selective agar and evaluation of antimicrobial resistance. J Cyst Fibros Dec 2011, 10(6):422-427.
79. Amin R., Waters V. Antibiotic treatment for Stenotrophomonas maltophilia in people with cystic fibrosis. Cochrane Database Syst Rev Apr 2 2014, 4:CD009249.
80. Barillova P., Tchesnokova V., Dubbers A., Kuster P., Peters G., Dobrindt U., et al. Prevalence and persistence of Escherichia coli in the airways of cystic fibrosis patients - an unrecognized CF pathogen?. Int J Med Microbiol May 2014, 304(3-4):415-421.
81. Cox M.J., Allgaier M., Taylor B., Baek M.S., Huang Y.J., Daly R.A., et al. Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PLoS One 2010, 5(6):e11044.
82. Rogers G.B., Carroll M.P., Serisier D.J., Hockey P.M., Jones G., Bruce K.D. 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.
83. Surette M.G. The cystic fibrosis lung microbiome. Ann Am Thorac Soc Jan 2014, 11(Suppl. 1):S61-S65.
84. van der Gast C.J., Walker A.W., Stressmann F.A., Rogers G.B., Scott P., Daniels T.W., et al. Partitioning core and satellite taxa from within cystic fibrosis lung bacterial communities. ISME J May 2011, 5(5):780-791.
85. Lynch S.V., Bruce K.D. The cystic fibrosis airway microbiome. Cold Spring Harb. Perspect. Med. Mar 2013, 3(3):a009738.
86. Rogers G.B., Carroll M.P., Serisier D.J., Hockey P.M., Jones G., Kehagia V., et al. Use of 16S rRNA gene profiling by terminal restriction fragment length polymorphism analysis to compare bacterial communities in sputum and mouthwash samples from patients with cystic fibrosis. J Clin Microbiol Jul 2006, 44(7):2601-2604.
87. Klepac-Ceraj V., Lemon K.P., Martin T.R., Allgaier M., Kembel S.W., Knapp A.A., et al. Relationship between cystic fibrosis respiratory tract bacterial communities and age, genotype, antibiotics and Pseudomonas aeruginosa. Environ Microbiol May 2010, 12(5):1293-1303.
88. Jung A., Kleinau I., Schonian G., Bauernfeind A., Chen C., Griese M., et al. Sequential genotyping of Pseudomonas aeruginosa from upper and lower airways of cystic fibrosis patients. Eur Respir J Dec 2002, 20(6):1457-1463.
89. Rogers G.B., Skelton S., Serisier D.J., van der Gast C.J., Bruce K.D. Determining cystic fibrosis-affected lung microbiology: comparison of spontaneous and serially induced sputum samples by use of terminal restriction fragment length polymorphism profiling. J Clin Microbiol Jan 2010, 48(1):78-86.
90. Harris J.K., De Groote M.A., Sagel S.D., Zemanick E.T., Kapsner R., Penvari C., et al. Molecular identification of bacteria in bronchoalveolar lavage fluid from children with cystic fibrosis. Proc Natl Acad Sci U S A Dec 18 2007, 104(51):20529-20533.
91. Carmody L.A., Zhao J., Schloss P.D., Petrosino J.F., Murray S., Young V.B., et al. Changes in cystic fibrosis airway microbiota at pulmonary exacerbation. Ann Am Thorac Soc Jun 2013, 10(3):179-187.
92. Fodor A.A., Klem E.R., Gilpin D.F., Elborn J.S., Boucher R.C., Tunney M.M., 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.
93. Zhao J., Murray S., Lipuma J.J. Modeling the impact of antibiotic exposure on human microbiota. Sci. Rep. 2014, 4:4345.
94. Stressmann F.A., Rogers G.B., van der Gast C.J., Marsh P., Vermeer L.S., Carroll M.P., et al. Long-term cultivation-independent microbial diversity analysis demonstrates that bacterial communities infecting the adult cystic fibrosis lung show stability and resilience. Thorax Oct 2012, 67(10):867-873.
95. Zhao J., Schloss P.D., Kalikin L.M., Carmody L.A., Foster B.K., Petrosino J.F., et al. Decade-long bacterial community dynamics in cystic fibrosis airways. Proc Natl Acad Sci U S A Apr 10 2012, 109(15):5809-5814.
96. Tunney M.M., Klem E.R., Fodor A.A., Gilpin D.F., Moriarty T.F., McGrath S.J., 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 Jul 2011, 66(7):579-584.
97. Daniels T.W., Rogers G.B., Stressmann F.A., van der Gast C.J., Bruce K.D., Jones G.R., et al. Impact of antibiotic treatment for pulmonary exacerbations on bacterial diversity in cystic fibrosis. J Cyst Fibros Jan 2013, 12(1):22-28.
98. Sibley C.D., Grinwis M.E., Field T.R., Parkins M.D., Norgaard J.C., Gregson D.B., et al. McKay agar enables routine quantification of the 'Streptococcus milleri' group in cystic fibrosis patients. J Med Microbiol May 2010, 59(Pt 5):534-540.
99. Sibley C.D., Parkins M.D., Rabin H.R., Duan K., Norgaard J.C., Surette M.G. A polymicrobial perspective of pulmonary infections exposes an enigmatic pathogen in cystic fibrosis patients. Proc Natl Acad Sci U S A Sep 30 2008, 105(39):15070-15075.
100. Britto M.T., Kotagal U.R., Hornung R.W., Atherton H.D., Tsevat J., Wilmott R.W. Impact of recent pulmonary exacerbations on quality of life in patients with cystic fibrosis. Chest Jan 2002, 121(1):64-72.
101. Lieu T.A., Ray G.T., Farmer G., Shay G.F. The cost of medical care for patients with cystic fibrosis in a health maintenance organization. Pediatrics Jun 1999, 103(6):e72.
102. Sanders D.B., Hoffman L.R., Emerson J., Gibson R.L., Rosenfeld M., Redding G.J., et al. Return of FEV1 after pulmonary exacerbation in children with cystic fibrosis. Pediatr Pulmonol Feb 2010, 45(2):127-134.
103. Mayer-Hamblett N., Rosenfeld M., Emerson J., Goss C.H., Aitken M.L. Developing cystic fibrosis lung transplant referral criteria using predictors of 2-year mortality. Am J Respir Crit Care Med Dec 15 2002, 166(12 Pt 1):1550-1555.
104. Liou T.G., Adler F.R., Cahill B.C., FitzSimmons S.C., Huang D., Hibbs J.R., et al. Survival effect of lung transplantation among patients with cystic fibrosis. JAMA Dec 5 2001, 286(21):2683-2689.
105. Parkins M.D., Sibley C.D., Surette M.G., Rabin H.R. The Streptococcus milleri group-an unrecognized cause of disease in cystic fibrosis: a case series and literature review. Pediatr Pulmonol May 2008, 43(5):490-497.
106. Hofstad T. Virulence factors in anaerobic bacteria. Eur J Clin Microbiol Infect Dis Nov 1992, 11(11):1044-1048.
107. Duerden B.I. Virulence factors in anaerobes. Clin Infect Dis May 1994, 18(Suppl. 4):S253-S259.
108. Sibley C.D., Duan K., Fischer C., Parkins M.D., Storey D.G., Rabin H.R., et al. Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections. PLoS Pathog Oct 2008, 4(10):e1000184.
109. Duan K., Dammel C., Stein J., Rabin H., Surette M.G. Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol Microbiol Dec 2003, 50(5):1477-1491.
110. Hajishengallis G., Liang S., Payne M.A., Hashim A., Jotwani R., Eskan M.A., et al. Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe Nov 17 2011, 10(5):497-506.
111. Sherrard L.J., Schaible B., Graham K.A., McGrath S.J., McIlreavey L., Hatch J., et al. Mechanisms of reduced susceptibility and genotypic prediction of antibiotic resistance in Prevotella isolated from cystic fibrosis (CF) and non-CF patients. J Antimicrob Chemother Jun 2014, 10.
112. Sherrard L.J., Graham K.A., McGrath S.J., McIlreavey L., Hatch J., Muhlebach M.S., et al. Antibiotic resistance in Prevotella species isolated from patients with cystic fibrosis. J Antimicrob Chemother Oct 2013, 68(10):2369-2374.
113. Grinwis M.E., Sibley C.D., Parkins M.D., Eshaghurshan C.S., Rabin H.R., Surette M.G. Macrolide and clindamycin resistance in Streptococcus milleri group isolates from the airways of cystic fibrosis patients. Antimicrob Agents Chemother Jul 2010, 54(7):2823-2829.
114. Sibley C.D., Parkins M.D., Rabin H.R., Surette M.G. The relevance of the polymicrobial nature of airway infection in the acute and chronic management of patients with cystic fibrosis. Curr Opin Investig Drugs Aug 2009, 10(8):787-794.
115. Tramper-Stranders G.A., Wolfs T.F., Fleer A., Kimpen J.L., van der Ent C.K. Maintenance azithromycin treatment in pediatric patients with cystic fibrosis: long-term outcomes related to macrolide resistance and pulmonary function. Pediatr Infect Dis J Jan 2007, 26(1):8-12.
116. Abstract 314: characterization of extended-spectrum β-lactamase production by Prevotella species from cystic fibrosis patients and detection of tem-type genes. The 28th Annual North American Cystic Fibrosis Conference 2014, [Atlanta, GA]. L. Sherrard, T. Matier, D. Gilpin, M. Muhlebach, J.S. Elborn, M. Tunney (Eds.).
117. Brook I. The role of beta-lactamase-producing-bacteria in mixed infections. BMC Infect Dis 2009, 9:202.
118. Wright G.D. The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol Mar 2007, 5(3):175-186.
119. Parkins M.D., Rendall J.C., Elborn J.S. Incidence and risk factors for pulmonary exacerbation treatment failures in patients with cystic fibrosis chronically infected with Pseudomonas aeruginosa. Chest Feb 2012, 141(2):485-493.
120. Canny G.O., McCormick B.A. Bacteria in the intestine, helpful residents or enemies from within?. Infect Immun Aug 2008, 76(8):3360-3373.
121. Casadevall A., Pirofski L.A. Host-pathogen interactions: redefining the basic concepts of virulence and pathogenicity. Infect Immun Aug 1999, 67(8):3703-3713.
122. Martin B., Schechter M.S., Jaffe A., Cooper P., Bell S.C., Ranganathan S. Comparison of the US and Australian cystic fibrosis registries: the impact of newborn screening. Pediatrics Feb 2012, 129(2):e348-e355.
123. Marzuillo C., De Giusti M., Tufi D., Giordano A., Del Cimmuto A., Quattrucci S., et al. Molecular characterization of Stenotrophomonas maltophilia isolates from cystic fibrosis patients and the hospital environment. Infect Control Hosp Epidemiol Aug 2009, 30(8):753-758.
124. Bryant J.M., Grogono D.M., Greaves D., Foweraker J., Roddick I., Inns T., et al. Whole-genome sequencing to identify transmission of Mycobacterium abscessus between patients with cystic fibrosis: a retrospective cohort study. Lancet May 4 2013, 381(9877):1551-1560.
125. Aaron S.D., Vandemheen K.L., Ramotar K., Giesbrecht-Lewis T., Tullis E., Freitag A., et al. Infection with transmissible strains of Pseudomonas aeruginosa and clinical outcomes in adults with cystic fibrosis. JAMA Nov 17 2010, 304(19):2145-2153.
126. Parkins M.D., Glezerson B.A., Sibley C.D., Sibley K.A., Duong J., Purighalla S., et al. Twenty-five-year outbreak of Pseudomonas aeruginosa infecting individuals with cystic fibrosis: identification of the prairie epidemic strain. J Clin Microbiol Apr 2014, 52(4):1127-1135.
127. Foweraker J.E., Laughton C.R., Brown D.F., Bilton D. Phenotypic variability of Pseudomonas aeruginosa in sputa from patients with acute infective exacerbation of cystic fibrosis and its impact on the validity of antimicrobial susceptibility testing. J Antimicrob Chemother Jun 2005, 55(6):921-927.
128. Li Z., Kosorok M.R., Farrell P.M., Laxova A., West S.E., Green C.G., et al. Longitudinal development of mucoid Pseudomonas aeruginosa infection and lung disease progression in children with cystic fibrosis. JAMA Feb 2 2005, 293(5):581-588.
129. Goerke C., Gressinger M., Endler K., Breitkopf C., Wardecki K., Stern M., et al. High phenotypic diversity in infecting but not in colonizing Staphylococcus aureus populations. Environ Microbiol Dec 2007, 9(12):3134-3142.
130. Knibbs L.D., Johnson G.R., Kidd T.J., Cheney J., Grimwood K., Kattenbelt J.A., et al. Viability of Pseudomonas aeruginosa in cough aerosols generated by persons with cystic fibrosis. Thorax Aug 2014, 69(8):740-745.
131. Wainwright C.E., France M.W., O'Rourke P., Anuj S., Kidd T.J., Nissen M.D., et al. Cough-generated aerosols of Pseudomonas aeruginosa and other Gram-negative bacteria from patients with cystic fibrosis. Thorax Nov 2009, 64(11):926-931.