Phenotypic and genotypic characterization of Stenotrophomonas maltophilia isolates from patients with cystic fibrosis: Genome diversity, biofilm formation, and virulence

BMC Microbiology

Volumn 11, Issue , 2011, Pages

  Pompilio, Arianna ^a   Pomponio, Stefano ^a   Crocetta, Valentina ^a   Gherardi, Giovanni ^b   Verginelli, Fabio ^a   Fiscarelli, Ersilia ^c   Dicuonzo, Giordano ^b   Savini, Vincenzo ^d   D'Antonio, Domenico ^d   Di Bonaventura, Giovanni ^a  

^a UNIVERSITY OF CHIETI   (Italy)

^b UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^c BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^d SPIRITO SANTO HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BIOFILM; CONTROLLED STUDY; CYSTIC FIBROSIS; FLAGELLUM; GENETIC SUSCEPTIBILITY; GENETIC TRAIT; GENETIC VARIABILITY; HUMAN; INFECTION; LUNG INFECTION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; POLYMERASE CHAIN REACTION; STENOTROPHOMONAS MALTOPHILIA; ANIMAL; BACTERIAL PNEUMONIA; CLASSIFICATION; CLUSTER ANALYSIS; DISEASE MODEL; FIMBRIA; GENETICS; GENOTYPE; GRAM NEGATIVE INFECTION; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; LOCOMOTION; MICROBIOLOGY; MOLECULAR TYPING; PATHOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PULSED FIELD GEL ELECTROPHORESIS; RODENT DISEASE; VIRULENCE;

BACTERIA (MICROORGANISMS); STENOTROPHOMONAS MALTOPHILIA;

ANIMALS; BIOFILMS; CLUSTER ANALYSIS; CYSTIC FIBROSIS; DISEASE MODELS, ANIMAL; ELECTROPHORESIS, GEL, PULSED-FIELD; FIMBRIAE, BACTERIAL; FLAGELLA; GENETIC VARIATION; GENOTYPE; GRAM-NEGATIVE BACTERIAL INFECTIONS; HUMANS; LOCOMOTION; MICE; MOLECULAR TYPING; OXIDATIVE STRESS; PHENOTYPE; PNEUMONIA, BACTERIAL; RODENT DISEASES; STENOTROPHOMONAS MALTOPHILIA; STRESS, PHYSIOLOGICAL; VIRULENCE;

EID: 79959845013     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-11-159     Document Type: Article

References (57)

1. The complete genome, comparative and functional analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants. LC Crossman VC Gould JM Dow GS Vernikos A Okazaki M Sebaihia D Saunders C Arrowsmith T Carver N Peters E Adlem A Kerhornou A Lord L Murphy K Seeger R Squares S Rutter MA Quail MA Rajandream D Harris C Churcher SD Bentley J Parkhill NR Thomson MB Avison, Genome Biol 2008 9 4 74 10.1186/gb-2008-9-4-r74 18419807
2. The molecular epidemiology of Stenotrophomonas maltophilia bacteraemia in a tertiary referral hospital in the United Arab Emirates 2000-2004. PA Jumaa A Sonnevend T Pl M El Hag R Amith O Trad, Ann Clin Microbiol Antimicrob 2006 5 32 10.1186/1476-0711-5-32 17194302
3. Emerging and unusual gram-negative infections in cystic fibrosis. JC Davies BK Rubin, Semin Respir Crit Care Med 2007 28 312 321 10.1055/s-2007- 981652 17562501 (Pubitemid 46982062)
4. Immunostimulatory properties of the emerging pathogen Stenotrophomonas maltophilia. VJ Waters MI Gámez G Soong S Amin RK Ernst A Prince, Infect Immun 2007 75 1698 1703 10.1128/IAI.01469-06 17220304 (Pubitemid 46559434)
5. Detecting Stenotrophomonas maltophilia does not reduce survival of patients with cystic fibrosis. CH Goss K Ott ML Aitken GD Rubenfeld, Am J Respir Crit Care Med 2002 166 356 361 10.1164/rccm.2109078 12153970 (Pubitemid 34864426)
6. Bacterial colonisation with Xanthomonas maltophilia - a retrospective study in a cystic fibrosis patient population. F Karpati AS Malmborg H Alfredsson L Hjelte B Strandvik, Infection 1994 22 258 263 10.1007/BF01739911 8002085 (Pubitemid 24255177)
7. Characterization of flagella produced by clinical strains of Stenotrophomonas maltophilia. D de Oliveira-Garcia M Dall'Agnol M Rosales AC Azzuz MB Martinez JA Girán, Emerg Infect Dis 2002 8 918 923 12194767 (Pubitemid 35000809)
8. Cytotoxic activity of clinical Stenotrophomonas maltophilia. PM Figueirêdo MT Furumura AM Santos AC Sousa DJ Kota CE Levy T Yano, Lett Appl Microbiol 2006 43 443 449 10.1111/j.1472-765X.2006.01965.x 16965377 (Pubitemid 44379191)
9. Detection of a phage genome carrying a zonula occludens like toxin gene (zot) in clinical isolates of Stenotrophomonas maltophilia. M Hagemann D Hasse G Berg, Arch Microbiol 2006 185 449 458 10.1007/s00203-006-0115-7 16775751 (Pubitemid 44072805)
10. Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. T Bjarnsholt P Jensen MJ Fiandaca J Pedersen CR Hansen CB Andersen T Pressler M Givskov N Høiby, Pediatr Pulmonol 2009 44 547 558 10.1002/ppul.21011 19418571
11. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. PK Singh AL Schaefer MR Parsek TO Moninger MJ Welsh EP Greenberg, Nature 2000 407 6805 762 764 10.1038/35037627 11048725
12. Biofilm formation by Stenotrophomonas maltophilia: modulation by quinolones, trimethoprim-sulfamethoxazole, and ceftazidime. G Di Bonaventura I Spedicato D D'Antonio I Robuffo R Piccolomini, Antimicrob Agents Chemother 2004 48 151 160 10.1128/AAC.48.1.151-160.2004 14693533 (Pubitemid 38040191)
13. Effect of environmental factors on biofilm formation by clinical Stenotrophomonas maltophilia isolates. G Di Bonaventura S Stepanovi C Picciani A Pompilio R Piccolomini, Folia Microbiol (Praha) 2007 52 86 90 10.1007/BF02932144 (Pubitemid 46631954)
14. Molecular characterization of virulence determinants of Stenotrophomonas maltophilia strains isolated from patients affected by cystic fibrosis. G Di Bonaventura G Prosseda F Del Chierico S Cannavacciuolo P Cipriani A Petrucca F Superti MG Ammendolia C Concato E Fiscarelli M Casalino R Piccolomini N Nicoletti B Colonna, Int J Immunopathol Pharmacol 2007 20 529 537 17880766 (Pubitemid 47531056)
15. Excessive inflammatory response of DBA/2 mice to Stenotrophomonas maltophilia lung infection: implications in cystic fibrosis. G Di Bonaventura A Pompilio R Zappacosta F Petrucci E Fiscarelli C Rossi R Piccolomini, Infect Immun 2010 78 2466 2476 10.1128/IAI.01391-09 20308302
16. Factors associated with adherence to and biofilm formation on polystyrene by Stenotrophomonas maltophilia: the role of cell surface hydrophobicity and motility. A Pompilio R Piccolomini C Picciani D D'Antonio V Savini G Di Bonaventura, FEMS Microbiol Lett 2008 287 41 47 10.1111/j.1574-6968.2008.01292.x 18681866
17. Adhesion to and biofilm formation on IB3-1 bronchial cells by Stenotrophomonas maltophilia isolates from cystic fibrosis patients. A Pompilio V Crocetta P Confalone M Nicoletti A Petrucca S Guarnieri E Fiscarelli V Savini R Piccolomini G Di Bonaventura, BMC Microbiol 2010 10 102 10.1186/1471-2180-10- 102 20374629
18. Diffusible signal factor-dependent cell-cell signaling and virulence in the nosocomial pathogen Stenotrophomonas maltophilia. Y Fouhy K Scanlon K Schouest C Spillane L Crossman MB Avison RP Ryan JM Dow, J Bacteriol 2007 189 4964 4968 10.1128/JB.00310-07 17468254 (Pubitemid 47025610)
19. Differential biofilm formation and motility associated with lipopolysaccharide/exopolysaccharide-coupled biosynthetic genes in Stenotrophomonas maltophilia. TP Huang EB Somers AC Wong, J Bacteriol 2006 188 3116 3120 10.1128/JB.188.8.3116-3120.2006 16585771
20. Role of phosphoglucomutase of Stenotrophomonas maltophilia in lipopolysaccharide biosynthesis, virulence, and antibiotic resistance. GA McKay DE Woods KL MacDonald K Poole, Infect Immun 2003 71 3068 3075 10.1128/IAI.71.6.3068-3075.2003 12761084 (Pubitemid 36637528)
21. Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia. M Denton KG Kerr, Clin Microbiol Rev 1998 11 57 80 9457429 (Pubitemid 28046016)
22. Use of random amplified polymorphic DNA PCR to examine epidemiology of Stenotrophomonas maltophilia and Achromobacter (Alcaligenes) xylosoxidans from patients with cystic fibrosis. JW Krzewinski CD Nguyen JM Foster JL Burns, J Clin Microbiol 2001 39 3597 3602 10.1128/JCM.39.10.3597-3602.2001 11574579 (Pubitemid 32954508)
23. Stenotrophomonas maltophilia strains from cystic fibrosis patients: genomic variability and molecular characterization of some virulence determinants. M Nicoletti A Iacobino G Prosseda E Fiscarelli R Zarrilli E De Carolis A Petrucca L Nencioni B Colonna M Casalino, Int J Med Microbiol 2011 301 1 34 43 10.1016/j.ijmm.2010.07.003 20952251
24. Persistence and variability of Stenotrophomonas maltophilia in cystic fibrosis patients, Madrid, 1991-1998. S Valdezate A Vindel L Maiz F Baquero H Escobar R Canton, Emerg Infect Dis 2001 7 113 122 10.3201/eid0701.010116 11266301 (Pubitemid 32173340)
25. High genetic diversity among Stenotrophomonas maltophilia strains despite their originating at a single hospital. S Valdezate A Vindel P Martin-Davila B Sanchez Del Saz F Baquero R Canton, J Clin Microbiol 2004 42 693 699 10.1128/JCM.42.2.693-699.2003 14766838 (Pubitemid 38222648)
26. A Stenotrophomonas maltophilia multilocus sequence typing scheme for inferring population structure. S Kaiser K Biehler D Jonas, J Bacteriol 2009 9 2934 2943
27. Molecular epidemiology of Stenotrophomonas maltophilia isolated from clinical specimens from patients with cystic fibrosis and associated environmental samples. M Denton NJ Todd KG Kerr PM Hawkey JM Littlewood, J Clin Microbiol 1998 36 1953 1958 9650943 (Pubitemid 28277783)
28. Genotypic and phenotypic relationships between clinical and environmental isolates of Stenotrophomonas maltophilia. G Berg N Roskot K Smalla, J Clin Microbiol 1999 37 3594 3600 10523559 (Pubitemid 29491099)
29. Antimicrobial susceptibility profile of molecular typed cystic fibrosis Stenotrophomonas maltophilia isolates and differences with noncystic fibrosis isolates. R Canton S Valdezate A Vindel B Sanchez Del Saz L Maiz F Baquero, Pediatr Pulmonol 2003 35 99 107 10.1002/ppul.10216 12526070 (Pubitemid 36177103)
30. Stenotrophomonas maltophilia: antimicrobial resistance and molecular typing of an emerging pathogen in a Turkish university hospital. D Gülmez G Hasçelik, Clin Microbiol Infect 2005 11 880 886 10.1111/j.1469-0691. 2005.01257.x 16216102 (Pubitemid 41535924)
31. Molecular typing of clinical isolates of Stenotrophomonas maltophilia by pulsed-field gel electrophoresis and random primer PCR fingerprinting. R Schaumann F Laurin AC Rodloff, Int J Hyg Environ Health 2008 211 3-4 292 298 10.1016/j.ijheh.2007.05.005 17980662 (Pubitemid 351847856)
32. Genotype and antibiotic susceptibility patterns of Pseudomonas aeruginosa and Stenotrophomonas maltophilia isolated from cystic fibrosis patients. H Nazik B Ongen Z Erturan M Salciolu, Jpn J Infect Dis 2007 60 82 86 17515637 (Pubitemid 47009521)
33. Molecular characterization of Stenotrophomonas maltophilia isolates from cystic fibrosis patients and the hospital environment. C Marzuillo M De Giusti D Tufi A Giordano A Del Cimmuto S Quattrucci C Mancini P Villari, Infect Control Hosp Epidemiol 2009 30 753 758 10.1086/598683 19583515
34. Environmental Stenotrophomonas maltophilia strain is less virulent than clinical strain from cystic fibrosis patient [Abstract]. A Pompilio V Crocetta S Pomponio A Bragonzi V Hol E Fiscarelli R Piccolomini G Di Bonaventura, Clin Microbiol Infect 2010 16 Suppl 2 590
35. Subinhibitory concentrations of moxifloxacin decrease adhesion and biofilm formation of Stenotrophomonas maltophilia from cystic fibrosis. A Pompilio C Catavitello C Picciani P Confalone R Piccolomini V Savini E Fiscarelli D D'Antonio G Di Bonaventura, J Med Microbiol 2010 59 Pt 1 76 81 19762476
36. The interaction between bacteria and bile. M Begley CGM Gahan C Hill, FEMS Microbiol Rev 2005 29 625 651 10.1016/j.femsre.2004.09.003 16102595 (Pubitemid 41139175)
37. Quorum-sensing regulation of gene expression: fundamental and applied aspects and the role in bacterial communication. IA Khmel, Microbiology 2006 75 390 397 10.1134/S0026261706040047 (Pubitemid 44174729)
38. Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. R Moxon C Bayliss D Hood, Annu Rev Genet 2006 40 307 333 10.1146/annurev.genet.40.110405.090442 17094739 (Pubitemid 44956788)
39. Pathogen evolution in vivo: genome dynamics of two isolates obtained 9 years apart from a duodenal ulcer patient infected with a single Helicobacter pylori strain. V Prouzet-Mauleon MA Hussain H Lamouliatte F Kauser F Megraud N Ahmed, J Clin Microbiol 2005 43 4237 4241 10.1128/JCM.43.8.4237-4241.2005 16081988 (Pubitemid 41129737)
40. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. E Drenkard FM Ausubel, Nature 2002 416 740 743 10.1038/416740a 11961556 (Pubitemid 34429150)
41. Nonmotility and phagocytic resistance of Pseudomonas aeruginosa isolates from chronically colonized patients with cystic fibrosis. E Mahenthiralingam ME Campbell DP Speert, Infect Immun 1994 62 596 605 8300217 (Pubitemid 24033780)
42. Random amplified polymorphic DNA typing of Pseudomonas aeruginosa isolates recovered from patients with cystic fibrosis. E Mahenthiralingam ME Campbell J Foster JS Lam DP Speert, J Clin Microbiol 1996 34 1129 1135 8727889 (Pubitemid 26126878)
43. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. D A Worlitzsch R Tarran M Ulrich U Schwab A Cekici KC Meyer P Birrer G Bellon J Berger T Weiss K Botzenhart JR Yankaskas S Randell RC Boucher G Doring, J Clin Invest 2002 109 317 325 11827991 (Pubitemid 34141805)
44. Heterogeneity of biofilms formed by nonmucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis. B Lee JA Haagensen O Ciofu JB Andersen N Høiby S Molin, J Clin Microbiol 2005 43 5247 5255 10.1128/JCM.43.10.5247-5255.2005 16207991 (Pubitemid 41484033)
45. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. GA O'Toole R Kolter, Mol Microbiol 1998 30 295 304 10.1046/j.1365-2958.1998.01062.x 9791175 (Pubitemid 28480181)
46. Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. M Klausen A Heydorn P Ragas L Lambertsen A Aaes- Jørgensen S Molin T Tolker-Nielsen, Mol Microbiol 2003 48 1511 1524 10.1046/j.1365-2958.2003.03525.x 12791135 (Pubitemid 36751058)
47. Biofilm formation by hyperpiliated mutants of Pseudomonas aeruginosa. P Chiang LL Burrows, J Bacteriol 2003 185 2374 2378 10.1128/JB.185.7.2374-2378. 2003 12644510 (Pubitemid 36363200)
48. Pseudomonas aeruginosa cystic fibrosis isolates of similar RAPD genotype exhibit diversity in biofilm forming ability in vitro. E Deligianni S Pattison D Berrar NG Ternan RW Haylock JE Moore SJ Elborn JS Dooley, BMC Microbiol 2010 8 38
49. Immunology of cystic fibrosis. G Döring R Knight G Bellon, Cystic fibrosis, Arnold, London, England, Hodson ME, Geddes D, 2000 109 141
50. Hydrogen peroxide and nitric oxide in exhaled air of children with cystic fibrosis during antibiotic treatment. Q Jobsis HC Raatgeep SL Schellekens A Kroesbergen WCJ Hop CJ de Jongste, Eur Respir J 2000 16 95 100 10.1034/j.1399-3003.2000.16a17.x 10933092 (Pubitemid 30480135)
51. Cross-sectional analysis of clinical and environmental isolates of Pseudomonas aeruginosa: biofilm formation, virulence, and genome diversity. NE Head H Yu, Infect Immun 2004 72 133 144 10.1128/IAI.72.1.133-144.2004 14688090 (Pubitemid 38018170)
52. Differential adaptation of microbial pathogens to airways of patients with cystic fibrosis and chronic obstructive pulmonary disease. G Döring IG Parameswaran TF Murphy, FEMS Microbiol Rev 2011 35 1 124 146 10.1111/j.1574-6976.2010.00237.x 20584083
53. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. S Stepanovi D Vukovi V Hola G Di Bonaventura S Djuki I Cirkovi F Ruzicka, APMIS 2007 115 891 899 10.1111/j.1600-0463.2007.apm-630.x 17696944 (Pubitemid 47260470)
54. Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. MH Rashid A Kornberg, Proc Natl Acad Sci USA 2000 97 4885 4890 10.1073/pnas.060030097 10758151 (Pubitemid 30238652)
55. Pseudomonas aeruginosa sodA and sodB mutants defective in manganese- and iron-cofactored superoxide dismutase activity demonstrate the importance of the iron-cofactored form in aerobic metabolism. DJ Hassett HP Schweizer DE Ohman, J Bacteriol 1995 177 6330 6337 7592406
56. Arlequin (version 3.0): an integrated software package for population genetics data analysis. L Excoffier G Laval S Schneider, Evol Bioinform Online 2005 1 47 50 19325852
57. Genetical structure of populations. S Wright, Nature 1950 166 4215 247 249 10.1038/166247a0 15439261