Evolution and diversification of Pseudomonas aeruginosa in the paranasal sinuses of cystic fibrosis children have implications for chronic lung infection

ISME Journal

Volumn 6, Issue 1, 2012, Pages 31-45

  Hansen, Susse Kirkelund ^a   Rau, Martin Holm ^a   Johansen, Helle Krogh ^b   Ciofu, Oana ^c   Jelsbak, Lars ^a   Yang, Lei ^a   Folkesson, Anders ^a   Jarmer, Hanne Østergaard ^a   Aanæs, Kasper ^b   Von Buchwald, Christian ^b   Høiby, Niels ^b,c   Molin, Søren ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b Rigshospitalet   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

adaptive evolution; chronic infection; cystic fibrosis; protected environment

Indexed keywords

ANTIBIOTIC RESISTANCE; BACTERIAL DISEASE; BACTERIUM; CHILD HEALTH; COLONIZATION; DISEASE TREATMENT; FITNESS; GENOTYPE; INFECTIVITY; OBSERVATIONAL METHOD; PATHOGENICITY; PHENOTYPE; SUBPOPULATION;

ADOLESCENT; ARTICLE; CHILD; CHRONIC DISEASE; CYSTIC FIBROSIS; EVOLUTION; GENETICS; HUMAN; ISOLATION AND PURIFICATION; LUNG; MICROBIOLOGY; MUTATION; PARANASAL SINUS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; RESPIRATORY TRACT INFECTION;

ADOLESCENT; BIOLOGICAL EVOLUTION; CHILD; CHRONIC DISEASE; CYSTIC FIBROSIS; HUMANS; LUNG; MUTATION; PARANASAL SINUSES; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RESPIRATORY TRACT INFECTIONS;

COPENHAGEN [(CTY) HOVEDSTADEN]; DENMARK; HOVEDSTADEN;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 84355161775     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2011.83     Document Type: Article

References (60)

1. Aanaes K, Rickelt LF, Johansen HK, von Buchwald C, Pressler T, Høiby N et al. (2011). Decreased mucosal oxygen tension in the maxillary sinuses in patients with cystic fibrosis. J Cyst Fibr 10: 114-120.
2. Andersen JB, Heydorn A, Hentzer M, Eberl L, Geisenberger O, Christensen BB et al. (2001). gfp-based N-acyl homoserine-lactone sensor systems for detection of bacterial communication. Appl Environ Microbiol 67: 575-585. (Pubitemid 32121344)
3. Boles BR, Thoendel M, Singh PK. (2005). Genetic variation in biofilms and the insurance effects of diversity. Microbiology 151: 2816-2818. (Pubitemid 41309555)
4. Brown MR, Foster JH. (1970). A simple diagnostic milk medium for Pseudomonas aeruginosa. J Clin Pathol 23: 172-177.
5. Burns JL, Gibson RL, McNamara S, Yim D, Emerson J, Rosenfeld M et al. (2001). Longitudinal assessment of Pseudomonas aeruginosa in young children with cystic fibrosis. J Infect Dis 183: 444-452. (Pubitemid 32105604)
6. Cabral DA, Loh BA, Speert DP. (1987). Mucoid Pseudomonas aeruginosa resists nonopsonic phagocytosis by human neutrophils and macrophages. Pediatr Res 22: 429-431. (Pubitemid 17146925)
7. Carenfelt C, Lundberg C. (1977). Purulent and nonpurulent maxillary sinus secretions with respect to pO2, pCO2 and pH. Acta Otolaryngol 84: 138-144. (Pubitemid 8110268)
8. Coste A, Gilain L, Roger G, Sebbagh G, Lenoir G, Manach Y et al. (1995). Endoscopic and CT-scan evaluation of rhinosinusitis in cystic fibrosis. Rhinology 33: 152-156.
9. D'Argenio DA, Wu M, Hoffman LR, Kulasekara HD, Deziel E, Smith EE et al. (2007). Growth phenotypes of Pseudomonas aeruginosa lasR mutants adapted to the airways of cystic fibrosis patients. Mol Microbiol 64: 512-533. (Pubitemid 46632635)
10. Dacheux D, Attree I, Toussaint B. (2001). Expression of ExsA in trans confers type III secretion systemdependent cytotoxicity on noncytotoxic Pseudomonas aeruginosa cystic fibrosis isolates. Infect Immun 69: 538-542. (Pubitemid 32038355)
11. Demko CA, Byard PJ, Davis PB. (1995). Gender differences in cystic fibrosis: Pseudomonas aeruginosa infection. J Clin Epidemiol 48: 1041-1049.
12. Deretic V, Schurr MJ, Yu H. (1995). Pseudomonas aeruginosa, mucoidy and the chronic infection phenotype in cystic fibrosis. Trends Microbiol 3: 351-356.
13. DeVries CA, Ohman DE. (1994). Mucoid-to-nonmucoid conversion in alginate-producing Pseudomonas aeruginosa often results from spontaneous mutations in algT, encoding a putative alternate sigma factor, and shows evidence for autoregulation. J Bacteriol 176: 6677-6687. (Pubitemid 24338083)
14. Doring G, Taccetti G, Campana S, Festini F, Mascherini M. (2006). Eradication of Pseudomonas aeruginosa in cystic fibrosis patients. Eur Respir J 27: 653. (Pubitemid 43372544)
15. Dosanjh A, Lakhani S, Elashoff D, Chin C, Hsu V, Hilman B. (2000). A comparison of microbiologic flora of the sinuses and airway among cystic fibrosis patients with maxillary antrostomies. Pediatr Transplant 4: 182-185. (Pubitemid 30471306)
16. Gibson RL, Emerson J, McNamara S, Burns JL, Rosenfeld M, Yunker A et al. (2003). Significant microbiological effect of inhaled tobramycin in young children with cystic fibrosis. Am J Respir Crit Care Med 167: 841-849. (Pubitemid 36801771)
17. Gysin C, Alothman GA, Papsin BC. (2000). Sinonasal disease in cystic fibrosis: clinical characteristics, diagnosis, and management. Pediatr Pulmonol 30: 481-489.
18. Hancock RE, Mutharia LM, Chan L, Darveau RP, Speert DP, Pier GB. (1983). Pseudomonas aeruginosa isolates from patients with cystic fibrosis: a class of serumsensitive, nontypable strains deficient in lipopolysaccharide O side chains. Infect Immun 42: 170-177. (Pubitemid 13012450)
19. Hansen SK, Rainey PB, Haagensen JA, Molin S. (2007). Evolution of species interactions in a biofilm community. Nature 445: 533-536. (Pubitemid 46197632)
20. Haussler S. (2004). Biofilm formation by the small colony variant phenotype of Pseudomonas aeruginosa. Environ Microbiol 6: 546-551. (Pubitemid 38708689)
21. Haussler S, Tummler B,Weissbrodt H, Rohde M, Steinmetz I. (1999). Small-colony variants of Pseudomonas aeruginosa in cystic fibrosis. Clin Infect Dis 29: 621-625. (Pubitemid 29439964)
22. Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR et al. (2002). Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148: 87-102. (Pubitemid 34083188)
23. Hoffman LR, Kulasekara HD, Emerson J, Houston LS, Burns JL, Ramsey BW et al. (2009). Pseudomonas aeruginosa lasR mutants are associated with cystic fibrosis lung disease progression. J Cyst Fibros 8: 66-70.
24. Hoffman LR, Richardson AR, Houston LS, Kulasekara HD, Martens-Habbena W, Klausen M et al. (2010). Nutrient availability as a mechanism for selection of antibiotic tolerant Pseudomonas aeruginosa within the CF airway. PLoS Pathogen 6: e1000712.
25. Høiby N. (1974). Epidemiological investigations of the respiratory tract bacteriology in patients with cystic fibrosis. Acta Pathol Microbiol Scand B 82: 541-550.
26. Høiby N. (1977). Pseudomonas aeruginosa infection in cystic fibrosis. Diagnostic and prognostic significance of pseudomonas aeruginosa precipitins determined by means of crossed immunoelectrophoresis. A survey. Scand J Respir Dis 58: 65-79.
27. Høiby N, Frederiksen B. (2000). Microbiology of cystic fibrosis. In: Hodson ME, Geddes DM (eds). Cystic Fibrosis, 2nd edn. Arnold: London, United Kingdom, pp 83-107.
28. Høiby N, Frederiksen B, Pressler T. (2005). Eradication of early Pseudomonas aeruginosa infection. J Cyst Fibros 4(Suppl 2): 49-54. (Pubitemid 41131329)
29. Høiby N, Pedersen SS. (1989). Estimated risk of cross-infection with Pseudomonas aeruginosa in Danish cystic fibrosis patients. Acta Paediatr Scand 78: 395-404. (Pubitemid 19133189)
30. Holloway BW, Morgan AF. (1986). Genome organization in Pseudomonas. Annu Rev Microbiol 40: 79-105.
31. Huxley EJ, Viroslav J, Gray WR, Pierce AK. (1978). Pharyngeal aspiration in normal adults and patients with depressed consciousness. Am J Med 64: 564-568. (Pubitemid 8322903)
32. Jelsbak L, Johansen HK, Frost AL, Thogersen R, Thomsen LE, Ciofu O et al. (2007). Molecular epidemiology and dynamics of Pseudomonas aeruginosa populations in lungs of cystic fibrosis patients. Infect Immun 75: 2214-2224. (Pubitemid 46744308)
33. Jones JW, Parsons DS, Cuyler JP. (1993). The results of functional endoscopic sinus (FES) surgery on the symptoms of patients with cystic fibrosis. Int J Pediatr Otorhinolaryngol 28: 25-32. (Pubitemid 24026090)
34. Koch C. (2002). Early infection and progression of cystic fibrosis lung disease. Pediatr Pulmonol 34: 232-236. (Pubitemid 34971079)
35. Lam J, Chan R, Lam K, Costerton JW. (1980). Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fibrosis. Infect Immun 28: 546-556. (Pubitemid 10102095)
36. Low AS, MacKenzie FM, Gould IM, Booth IR. (2001). Protected environments allow parallel evolution of a bacterial pathogen in a patient subjected to long-term antibiotic therapy. Mol Microbiol 42: 619-630. (Pubitemid 33064474)
37. Mahenthiralingam E, Campbell ME, Speert DP. (1994). Nonmotility and phagocytic resistance of Pseudomonas aeruginosa isolates from chronically colonized patients with cystic fibrosis. Infect Immun 62: 596-605. (Pubitemid 24033780)
38. Mainz JG, Naehrlich L, Schien M, Kading M, Schiller I, Mayr S et al. (2009). Concordant genotype of upper and lower airways P aeruginosa and S. aureus isolates in cystic fibrosis. Thorax 64: 535-540.
39. Muhlebach MS, Miller MB, Moore C, Wedd JP, Drake AF, Leigh MW. (2006). Are lower airway or throat cultures predictive of sinus bacteriology in cystic fibrosis? Pediatr Pulmonol 41: 445-451. (Pubitemid 43673064)
40. Munck A, Bonacorsi S, Mariani-Kurkdjian P, Lebourgeois M, Gerardin M, Brahimi N et al. (2001). Genotypic characterization of Pseudomonas aeruginosa strains recovered from patients with cystic fibrosis after initial and subsequent colonization. Pediatr Pulmonol 32: 288-292. (Pubitemid 32938877)
41. Nguyen D, Singh PK. (2006). Evolving stealth: genetic adaptation of Pseudomonas aeruginosa during cystic fibrosis infections. Proc Natl Acad Sci USA 103: 8305-8306. (Pubitemid 43838449)
42. Nishioka GJ, Barbero GJ, Konig P, Parsons DS, Cook PR, Davis WE. (1995). Symptom outcome after functional endoscopic sinus surgery in patients with cystic fibrosis: a prospective study. Otolaryngol Head Neck Surg 113: 440-445.
43. Parad RB, Gerard CJ, Zurakowski D, Nichols DP, Pier GB. (1999). Pulmonary outcome in cystic fibrosis is influenced primarily by mucoid Pseudomonas aeruginosa infection and immune status and only modestly by genotype. Infect Immun 67: 4744-4750. (Pubitemid 29400459)
44. Poole K. (2004). Efflux-mediated multiresistance in Gramnegative bacteria. Clin Microbiol Infect 10: 12-26.
45. Pratt LA, Kolter R. (1998). Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 30: 285-293. (Pubitemid 28480180)
46. Rainey PB, Travisano M. (1998). Adaptive radiation in a heterogeneous environment. Nature 394: 69-72. (Pubitemid 28321802)
47. Rau MH, Hansen SK, Johansen HK, Thomsen LE, Workman CT, Nielsen KF et al. (2010). Early adaptive developments of Pseudomonas aeruginosa after the transition from life in the environment to persistent colonization in the airways of human cystic fibrosis hosts. Environ Microbiol 12: 1643-1658.
48. Robertson JM, Friedman EM, Rubin BK. (2008). Nasal and sinus disease in cystic fibrosis. Paediatr Respir Rev 9: 213-219.
49. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, D'Argenio DA et al. (2006). Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 103: 8487-8492. (Pubitemid 43838482)
50. Starkey M, Hickman JH, Ma L, Zhang N, De Long S, Hinz A et al. (2009). Pseudomonas aeruginosa rugose small-colony variants have adaptations that likely promote persistence in the cystic fibrosis lung. J Bacteriol 191: 3492-3503.
51. Taccetti G, Campana S, Festini F, Mascherini M, Doring G. (2005). Early eradication therapy against Pseudomonas aeruginosa in cystic fibrosis patients. Eur Respir J 26: 458-461. (Pubitemid 41264209)
52. Taylor RF, Morgan DW, Nicholson PS, Mackay IS, Hodson ME, Pitt TL. (1992). Extrapulmonary sites of Pseudomonas aeruginosa in adults with cystic fibrosis. Thorax 47: 426-428.
53. Terry JM, Pina SE, Mattingly SJ. (1991). Environmental conditions which influence mucoid conversion Pseudomonas aeruginosa PAO1. Infect Immun 59: 471-477.
54. Terry JM, Pina SE, Mattingly SJ. (1992). Role of energy metabolism in conversion of nonmucoid Pseudomonas aeruginosa to the mucoid phenotype. Infect Immun 60: 1329-1335.
55. Thomassen MJ, Demko CA, Boxerbaum B, Stern RC, Kuchenbrod PJ. (1979). Multiple of isolates of Pseudomonas aeruginosa with differing antimicrobial susceptibility patterns from patients with cystic fibrosis. J Infect Dis 140: 873-880. (Pubitemid 10165125)
56. Wahba AH, Darrell JH. (1965). The identification of atypical strains of Pseudomonas aeruginosa. J Gen Microbiol 38: 329-342.
57. Wiehlmann L, Wagner G, Cramer N, Siebert B, Gudowius P, Morales G et al. (2007). Population structure of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 104: 8101-8106. (Pubitemid 47185882)
58. Yang L, Haagensen JA, Jelsbak L, Johansen HK, Sternberg C, Høiby N et al. (2008). In situ growth rates and biofilm development of Pseudomonas aeruginosa populations in chronic lung infections. J Bacteriol 190: 2767-2776. (Pubitemid 351508176)
59. Yang L, Jelsbak L, Marvig RL, Damkiær S, Workman CT, Rau MH et al. (2011). Evolutionary dynamics of bacteria in a human host environment. Proc Natl Acad Sci USA 108: 7481-7466.
60. Yang L, Rybtke MT, Jakobsen TH, Hentzer M, Bjarnsholt T, Givskov M et al. (2009). Computer-aided identification of recognized drugs as Pseudomonas aeruginosa quorum-sensing inhibitors. Antimicrob Agents Chemother 53: 2432-2443.