Clonal Dissemination, Emergence of Mutator Lineages and Antibiotic Resistance Evolution in Pseudomonas aeruginosa Cystic Fibrosis Chronic Lung Infection

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  López Causapé, Carla ^a   Rojo Molinero, Estrella ^a   Mulet, Xavier ^a   Cabot, Gabriel ^a   Moyà, Bartolomé ^a   Figuerola, Joan ^a   Togores, Bernat ^a   Pérez, José L ^a   Oliver, Antonio ^a  

^a HOSPITAL UNIVERSITARIO SON ESPASES   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AZTREONAM; BETA LACTAMASE AMPC; CEFEPIME; CEFTAZIDIME; CIPROFLOXACIN; COLISTIN; IMIPENEM; MEROPENEM; MEXB PROTEIN; MEXD PROTEIN; MEXF PROTEIN; MEXY PROTEIN; MULTIDRUG RESISTANCE PROTEIN; RIFAMPICIN; TOBRAMYCIN; UNCLASSIFIED DRUG;

ALLELE; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIUM ISOLATE; CONTROLLED STUDY; CORRELATION ANALYSIS; CYSTIC FIBROSIS; GENE MUTATION; GENETIC ANALYSIS; GENETIC VARIABILITY; GENOTYPE; LUNG INFECTION; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR CLONING; MULTILOCUS SEQUENCE TYPING; NONHUMAN; POINT MUTATION; PSEUDOMONAS AERUGINOSA; PULSED FIELD GEL ELECTROPHORESIS; RESTRICTION FRAGMENT; SPAIN;

ALLELES; ANTI-BACTERIAL AGENTS; CYSTIC FIBROSIS; DRUG RESISTANCE, BACTERIAL; ELECTROPHORESIS, GEL, PULSED-FIELD; HUMANS; MICROBIAL SENSITIVITY TESTS; MULTILOCUS SEQUENCE TYPING; MUTATION; PHENOTYPE; PNEUMONIA, BACTERIAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS;

EID: 84881513008     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071001     Document Type: Article

References (50)

1. Lyczak JB, Cannon CL, Pier GB, (2002) Lung infection associated with cystic fibrosis. Clin Microbiol Rev 15: 194-222.
2. Gibson RL, Burns JL, Rammsey BW, (2003) Pathophysiology and management of pulmonary infections in cystic fibrosis. Am J Respir Crit Care Med 168: 918-951.
3. Burns JL, Gibson RL, McNamara S, Yim D, Emerson J, et al. (2001) Longitudinal assessment of Pseudomonas aeruginosa in young children with cystic fibrosis. J Infect Dis 183: 444-52.
4. Costerton J, Stewart P, Greenberg E, (1999) Bacterial biofilms: a common cause of persistent infections. Science 284: 1318-1322.
5. Smith EE, Buckley DG, Wu Z, Saenphimmachack C, Hoffman LR, et al. (2006) Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 103: 8487-8492.
6. Hogardt M, Heesemann J, (2010) Adaptation of Pseudomonas aeruginosa during persistence in the CF lung. Int J Med Microbiol 300: 557-532.
7. Hauser AR, Jain M, Bar-Meir M, McColley SA, (2011) Clinical significance of microbial infection and adaptation in cystic fibrosis. Clin Microbiol Rev 24: 29-70.
8. Bragonzi A, Paroni M, Nonis A, Cramer N, Montanari S, et al. (2009) Pseudomonas aeruginosa microevolution during cystic fibrosis lung infection establishes clones with adapted virulence. Am J Respir Crit Care Med 180: 138-45.
9. Rodríguez-Rojas A, Oliver A, Blázquez J, (2012) Intrinsic and environmental mutagenesis drive diversification and persistence of Pseudomonas aeruginosa in chronic lung infections. J Infect Dis 205: 121-7.
10. Oliver A, Cantón R, Campo P, Baquero F, Blázquez J, (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288: 1251-4.
11. Ciofu O, Riis B, Pressler T, Poulsen HE, Hoiby N, (2005) Occurrence of hypermutable Pseudomonas aeruginosa in cystic fibrosis patients is associated with the oxidative stress caused by chronic lung inflammation. Antimicrob Agents Chemother 49: 2276-2282.
12. Oliver A, Mena A, (2010) Bacterial hypermutation in cystic fibrosis, not only for antibiotic resistance. Clin Microbiol Infect 16: 798-808.
13. Oliver A, (2010) Mutators in cystic fibrosis chronic lung infection: Prevalence, mechanisms, and consequences for antimicrobial therapy. Int J Med Microbiol 300: 563-72.
14. Oliver A, Baquero F, Blázquez J, (2002) The mismatch repair system (mutS, mutL and uvrD genes) in Pseudomonas aeruginosa: molecular characterization of naturally occurring mutants. Mol Microbiol 43: 641-50.
15. Mena A, Smith EE, Burns JL, Speert DP, Moskowitz SM, et al. (2008) Genetic adaptation of Pseudomonas aeruginosa to the airways of cystic fibrosis patients is catalyzed by hypermutation. J Bacteriol 190: 7910-7.
16. Feliziani S, Luján AM, Moyano AJ, Sola C, Bocco JL, (2010) Mucoidy, quorum sensing, mismatch repair and antibiotic resistance in Pseudomonas aeruginosa from cystic fibrosis chronic airways infections. PLoS One 5: e12669.
17. Luján AM, Maciá MD, Yang L, Molin S, Oliver A, et al. (2011) Evolution and adaptation in Pseudomonas aeruginosa biofilms driven by mismatch repair system-deficient mutators. PLoS One 6: e27842.
18. Hoboth C, Hoffmann R, Eichner A, Henke C, Schmoldt S, (2009) Dynamics of adaptive microevolution of hypermutable Pseudomonas aeruginosa during chronic pulmonary infection in patients with cystic fibrosis. J Infect Dis 200: 118-130.
19. Ferroni A, Guillemot D, Moumile K, Bernede C, Le Bourgeois M, et al. (2009) Effect of mutatorP. aeruginosa on antibiotic resistance acquisition and respiratory function in cystic fibrosis. Pediatr Pulmonol 44: 820-5.
20. Henrichfreise B, Wiegand I, Pfister W, Wiedemann B, (2007) Resistance mechanisms of multiresistant Pseudomonasaeruginosa strains from Germany and correlation with hypermutation. Antimicrob Agents Chemother 51: 4062-70.
21. Folkesson A, Jelsbak L, Yang L, Johansen HK, Ciofu O, et al. (2012) Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat Rev Microbiol 10: 41-51.
22. Cramer N, Wiehlmann L, Tummler B, (2010) Clonal epidemiology of Pseudomonas aeruginosa in cystic fibrosis. Int J Med Microbiol 300: 526-533.
23. Cramer N, Wielhlmann L, Ciofu O, Tamm S, Hoiby N, et al. (2012) Molecular epidemiology of chronic Pseudomonas aeruginosa airway infections in cystic fibrosis. PLoS One 7: e50731.
24. Kenna DT, Doherty CJ, Foweraker J, Macaskill L, Barcus VA, et al. (2007) Hypermutability in environmental Pseudomonas aeruginosa and in populations causing pulmonary infection in individuals with cystic fibrosis. Microbiology 153: 1852-9.
25. Mowat E, Paterson S, Fothergill JL, Wright EA, Ledson MJ, et al. (2011) Pseudomonas aeruginosa population diversity and turnover in cystic fibrosis chronic infections. Am J RespirCrit Care Med 183: 1674-9.
26. Yang L, Jelsbak L, Marvig RL, Damkiær S, Workman CT, et al. (2011) Evolutionary dynamics of bacteria in a human host environment. Proc Natl Acad Sci USA 108: 481-6.
27. Römling U, Grothues D, Heuer T, Tümmler B, (1992) Physical genome analysis of bacteria. Electrophoresis 13: 626-631.
28. Fothergill JL, White J, Foweraker JE, Walshaw MJ, Ledson MJ, et al. (2010) Impact of Pseudomonas aeruginosa genomic instability on the application of typing methods for chronic cystic fibrosis infections. J ClinMicrobiol 48: 2053-9.
29. Curran B, Jonas D, Grundmann H, Pitt T, Dowson CG, (2004) Development of a multilocus sequence typing scheme for the opportunistic pathogen Pseudomonas aeruginosa. J Clin Microbiol 42: 5644-9.
30. Kidd TJ, Grimwood K, Ramsay KA, Rainey P, Bell SC, (2011) Comparison of three molecular techniques for typing Pseudomonas aeruginosa isolates in sputum samples. J Clin Microbiol 49: 263-268.
31. Férnandez-Olmos A, García-Castillo M, Alba JM, Morosini MI, Lamas A, et al. (2013) Population structure and antimicrobial susceptibility of both non-persistent and persistent Pseudomonas aeruginosa isolates recovered in cystic fibrosis patients. J Clin Microbiol. In press.
32. Cabot G, Ocampo-Sosa AA, Domínguez MA, Gago JF, Juan C, et al. (2012) Genetic markers of widespread extensively drug-resistant Pseudomonas aeruginosa high-risk clones. Antimicrob Agents Chemother 56: 6349-57.
33. García-Castillo M, Del Campo R, Morosini MI, Riera E, Cabot G, et al. (2011) Wide dispersion of ST175 clone despite high genetic diversity of carbapenem-nonsusceptible Pseudomonas aeruginosa clinical strains in 16 Spanish hospitals. J Clin Microbiol 49: 2905-10.
34. Warren AE, Boulianne-Larsen CM, Chandler CB, Chiotti K, Kroll E, et al. (2011) Genotypic and phenotypic variation in Pseudomonas aeruginosa reveals signatures of secondary infection and mutator activity in certain cystic fibrosis patients with chronic lung infections. Infect Immun 79: 4802-4818.
35. García-Castillo M, Máiz L, Morosini MI, Rodríguez-Baños M, Suarez L, et al. (2012) Emergence of a mutL mutation causing multilocus sequence typing-pulsed-field gel electrophoresis discrepancy among Pseudomonas aeruginosa isolates from a cystic fibrosis patient. J Clin Microbiol 50: 1777-8.
36. Kidd TJ, Ritchie SR, Ramsay KA, Grimwood K, Bell SC, et al. (2012) Pseudomonas aeruginosa exhibits frequent recombination, but only a limited association between genotype and ecological setting. PLoS One 7: e44199.
37. Salunkhe P, Smart CH, Morgan JA, Panagea S, Walshaw MJ, et al. (2005) A cystic fibrosis epidemic strain of Pseudomonas aeruginosa displays enhanced virulence and antimicrobial resistance J Bacteriol. 187: 4908-20.
38. Hogardt M, Schubert S, Adler K, Götzfried M, Heesemann J, (2006) Sequence variability and functional analysis of MutS of hypermutable Pseudomonasaeruginosa cystic fibrosis isolates. Int J Med Microbiol 296: 313-20.
39. Montanari S, Oliver A, Salerno P, Mena A, Bertoni G, et al. (2007) Biological cost of hypermutation in Pseudomonas aeruginosa strains from patients with cystic fibrosis. Microbiology 153: 1445-54.
40. Parkins MD, Elborn JS, (2010) Aztreonam lysine: a novel inhalational antibiotic for cystic fibrosis. Expert Rev Respir Med 4: 435-44.
41. Macia MD, Blanquer D, Togores B, Sauleda J, Perez JL, et al. (2005) Hypermutation is a key factor in development of multiple-antimicrobial resistance in Pseudomonas aeruginosa strains causing chronic lung infections. Antimicrob Agents Chemother 49: 3382-3386.
42. Wolter DJ, Black JA, Lister PD, Hanson ND, (2009) Multiple genotypic changes in hypersusceptible strains of Pseudomonas aeruginosa isolated from cystic fibrosis patients do not always correlate with the phenotype. J Antimicrob Chemother 64: 294-300.
43. Tomás M, Doumith M, Warner M, Turton JF, Beceiro A, et al. (2010) Efflux pumps, OprD porin, AmpC beta-lactamase, and multiresistance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Antimicrob Agents Chemother 54: 2219-24.
44. Vettoretti L, Plésiat P, Muller C, El Garch F, Phan G, et al. (2009) Efflux unbalance in Pseudomonasaeruginosa isolates from cystic fibrosis patients. Antimicrob Agents Chemother 53: 1987-97.
45. Mulet X, Moyà B, Juan C, Maciá MD, Pérez JL, et al. (2011) Antagonistic interactions of Pseudomonas aeruginosa antibiotic resistance mechanisms in planktonic but not biofilm growth. Antimicrob Agents Chemother 55: 4560-4568.
46. Vogne C, Aires JR, Bailly C, Hocquet D, Plésiat P, (2004) Role of the multidrug efflux system MexXY in the emergence of moderate resistance to aminoglycosides among Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Antimicrob Agents Chemother 48: 1676-80.
47. Kaufmann ME, (1998) Pulsed-field gel electrophoresis. Methods Mol Med 15: 33-50.
48. Tenover FC, Arbeit RD, Goering RV, Mickelsen A, Murray BE, et al. (1995) Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol33: 2233-2239.
49. Oh H, Stenhoff J, Jalal S, Wretlind B, (2003) Role of efflux pumps and mutations in genes for topoisomerases II and IV in fluoroquinolone-resistant Pseudomonas aeruginosa strains. Microb Drug Resist 8: 323-328.
50. Cabot G, Ocampo-Sosa AA, Tubau F, Maciá MD, Rodríguez C, et al. (2011) Overexpression of AmpC and efflux pumps in Pseudomonas aeruginosa isolates from bloodstream infections: prevalence and impact on resistance in a Spanish multicenter study. Antimicrob Agents Chemother 55: 1906-11.