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Identification, molecular characterisation and antimicrobial susceptibility of genomovars of the Burkholderia cepacia complex in Spain

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Abstract

Burkholderia spp. strains collected in Spain over a 13-year period from patients with cystic fibrosis (CF) (n = 148), non-CF patients (n = 103) and from environmental sources (n = 64) were characterised. One hundred and forty-one of the examined strains were involved in seven suspected nosocomial disease outbreaks. Strains were identified by their 16s rRNA and recA genes. Their genetic relatedness, the possession of cable pili and the B. cepacia epidemic strain marker (BCESM), and their susceptibility to antimicrobial agents were studied using pulsed-field gel electrophoresis (PFGE), cblA and esmR genes analysis, and by the E-test, respectively. The genomovar distribution for the 315 strains was as follows: B. stabilis 29.5 %, B. cepacia 14.9 %, B. multivorans 11.1 %, B. cenocepacia IIIA 9.5 %, B. vietnamiensis 3.8 %, B. cenocepacia IIIB 3.5 %, and B. ambifaria and B. pyrrocinia 0.3 % each. The genetic diversity of the B. cepacia complex (Bcc) was ample, with 57 different SpeI types, showing a genetic similarity of 36.4–96.6 %. No strain carried cblA, whereas 25 B. cenocepacia genotypes harboured BCESM (23 from patients with CF). Antimicrobial resistance rates to tobramycin (TOB; 86 %) and imipenem (IPM; 67 %) were high. The strains from patients with CF showed significantly greater resistance to piperacillin (PIP), levofloxacin (LVX) and co-trimoxazole (SXT) than those isolated from non-CF patients (p < 0.05). In conclusion, B. cenocepacia was the most prevalent genomovar found in patients with CF (19.1 %), whereas B. cepacia was the most common among non-CF patients (20.7 %). B. stabilis (47.6 %) was the most common environmental genomovar. Susceptibility to antimicrobial agents depended on genomovar status and strain origin.

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References

  1. Vandamme P, Holmes B, Vancanneyt M, Coenye T, Hoste B, Coopman R, Revets H, Lauwers S, Gillis M, Kersters K, Govan JRW (1997) Occurrence of multiple genomovars of Burkholderia cepacia in cystic fibrosis patients and proposal of Burkholderia multivorans sp. nov. Int J Syst Bacteriol 47:1188–1200

    Article  PubMed  CAS  Google Scholar 

  2. Vandamme P, Holmes B, Coenye T, Goris J, Mahenthiralingam E, Lipuma JJ, Govan JRW (2003) Burkholderia cenocepacia sp. nov.—a new twist to an old story. Res Microbiol 154:91–96

    Article  PubMed  Google Scholar 

  3. Vandamme P, Mahenthiralingam E, Holmes B, Coenye T, Hoste B, De Vos P, Henry D, Speert DP (2000) Identification and population structure of Burkholderia stabilis sp. nov. (formerly Burkholderia cepacia genomovar IV). J Clin Microbiol 38:1042–1047

    PubMed  CAS  Google Scholar 

  4. Gillis M, Van Van T, Bardin R, Goor M, Hebbar P, Willems A, Segers P, Kersters K, Heulin T, Fernandez MP (1995) Polyphasic taxonomy in the genus Burkholderia leading to an emended description of the genus and proposition of Burkholderia vietnamiensis sp. nov. for N2-fixing isolates from rice in Vietnam. Int J Syst Bacteriol 45:274–289

    Article  CAS  Google Scholar 

  5. Vermis K, Coenye T, Lipuma JJ, Mahenthiralingam E, Nelis HJ, Vandamme P (2004) Proposal to accommodate Burkholderia cepacia genomovar VI as Burkholderia dolosa sp. nov. Int J Syst Evol Microbiol 54:689–691

    Article  PubMed  CAS  Google Scholar 

  6. Coenye T, Mahenthiralingam E, Henry D, LiPuma JJ, Laevens S, Gillis M, Speert DP, Vandamme P (2001) Burkholderia ambifaria sp. nov., a novel member of the Burkholderia cepacia complex including biocontrol and cystic fibrosis-related isolates. Int J Syst Evol Microbiol 51:1481–1490

    Article  PubMed  CAS  Google Scholar 

  7. Vandamme P, Henry D, Coenye T, Nzula S, Vancanneyt M, Lipuma JJ, Speert DP, Govan JRW, Mahenthiralingam E (2002) Burkholderia anthina sp. nov. and Burkholderia pyrrocinia, two additional Burkholderia cepacia complex bacteria, may confound results of new molecular diagnostic tools. FEMS Immunol Med Microbiol 33:143–149

    Article  PubMed  CAS  Google Scholar 

  8. Yabuuchi E, Kawamura Y, Ezaki T, Ikedo M, Dejsirilert S, Fujiwara N, Naka T, Kobayashi K (2000) Burkholderia uboniae sp. nov., L-arabinose-assimilating but different from Burkholderia thailandensis and Burkholderia vietnamiensis. Microbiol Immunol 44:307–317

    PubMed  CAS  Google Scholar 

  9. Vermis K, Coenye T, Mahenthiralingam E, Nelis HJ, Vandamme P (2002) Evaluation of species-specific recA-based PCR tests for genomovar level identification within the Burkholderia cepacia complex. J Med Microbiol 51:937–940

    PubMed  CAS  Google Scholar 

  10. Vanlaere E, Lipuma JJ, Baldwin A, Henry D, De Brandt E, Mahenthiralingam E, Speert D, Dowson C, Vandamme P (2008) 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 58:1580–1590

    Article  PubMed  CAS  Google Scholar 

  11. Vanlaere E, Baldwin A, Gevers D, Henry D, De Brandt E, Lipuma JJ, Mahenthiralingam E, Speert DP, Dowson C, Vandamme P (2009) Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol 59:102–111

    Article  PubMed  CAS  Google Scholar 

  12. Gilligan PH (1991) Microbiology of airway disease in patients with cystic fibrosis. Clin Microbiol Rev 4:35–51

    PubMed  CAS  Google Scholar 

  13. Winkelstein JA, Marino MC, Johnston RB Jr, Boyle J, Curnutte J, Gallin JI, Malech HL, Holland SM, Ochs H, Quie P, Buckley RH, Foster CB, Chanock SJ, Dickler H (2000) Chronic granulomatous disease. Report on a national registry of 368 patients. Medicine (Baltimore) 79:155–169

    Article  CAS  Google Scholar 

  14. Clode FE, Kaufmann ME, Malnick H, Pitt TL (2000) Distribution of genes encoding putative transmissibility factors among epidemic and nonepidemic strains of Burkholderia cepacia from cystic fibrosis patients in the United Kingdom. J Clin Microbiol 38:1763–1766

    PubMed  CAS  Google Scholar 

  15. Gilligan PH, Lum G, Vandamme AR, Whittier S (2003) Burkholderia, Stenotrophomonas, Ralstonia, Brevundimonas, Comamonas, Delftia, Pandoraea, and Acidovorax. In: Murray PR, Baron EJ, Jorgensen JH, Pfaller MA, Yolken RH (eds) Manual of clinical microbiology, 8th edn. ASM Press, Washington, DC, pp 729–748

    Google Scholar 

  16. Mahenthiralingam E, Urban TA, Goldberg JB (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3:144–156

    Article  PubMed  CAS  Google Scholar 

  17. Nzula S, Vandamme P, Govan JRW (2002) Influence of taxonomic status on the in vitro antimicrobial susceptibility of the Burkholderia cepacia complex. J Antimicrob Chemother 50:265–269

    Article  PubMed  CAS  Google Scholar 

  18. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    PubMed  CAS  Google Scholar 

  19. Mahenthiralingam E, Bischof J, Byrne SK, Radomski C, Davies JE, Av-Gay Y, Vandamme P (2000) DNA-based diagnostic approaches for identification of Burkholderia cepacia complex, Burkholderia vietnamiensis, Burkholderia multivorans, Burkholderia stabilis, and Burkholderia cepacia genomovars I and III. J Clin Microbiol 38:3165–3173

    PubMed  CAS  Google Scholar 

  20. Valdezate S, Vindel A, Maiz L, Baquero F, Escobar H, Cantón R (2001) Persistence and variability of Stenotrophomonas maltophilia in cystic fibrosis patients, Madrid, 1991–1998. Emerg Infect Dis 7:113–122

    Article  PubMed  CAS  Google Scholar 

  21. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, Swaminathan B (1995) Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33:2233–2239

    PubMed  CAS  Google Scholar 

  22. National Committee for Clinical Laboratory Standards (NCCLS) (2007) Performance standards for antimicrobial susceptibility testing; Seventeenth Informational Supplement. M100-S17. NCCLS, Wayne, PA

  23. Drancourt M, Bollet C, Carlioz A, Martelin R, Gayral JP, Raoult D (2000) 16S ribosomal DNA sequence analysis of a large collection of environmental and clinical unidentifiable bacterial isolates. J Clin Microbiol 38:3623–3630

    PubMed  CAS  Google Scholar 

  24. Molina-Cabrillana J, Bolaños-Rivero M, Alvarez-León EE, Martín Sánchez AM, Sánchez-Palacios M, Alvarez D, Sáez-Nieto JA (2006) Intrinsically contaminated alcohol-free mouthwash implicated in a nosocomial outbreak of Burkholderia cepacia colonization and infection. Infect Control Hosp Epidemiol 27:1281–1282

    Article  PubMed  Google Scholar 

  25. Bernhardt SA, Spilker T, Coffey T, LiPuma JJ (2003) Burkholderia cepacia complex in cystic fibrosis: frequency of strain replacement during chronic infection. Clin Infect Dis 37:780–785

    Article  PubMed  Google Scholar 

  26. McDowell A, Mahenthiralingam E, Dunbar KEA, Moore JE, Crowe M, Elborn JS (2004) Epidemiology of Burkholderia cepacia complex species recovered from cystic fibrosis patients: issues related to patient segregation. J Med Microbiol 53:663–668

    Article  PubMed  CAS  Google Scholar 

  27. Mahenthiralingam E, Baldwin A, Dowson CG (2008) Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol 104:1539–1551

    Article  PubMed  CAS  Google Scholar 

  28. Heath DG, Hohneker K, Carriker C, Smith K, Routh J, LiPuma JJ, Aris RM, Weber D, Gilligan PH (2002) Six-year molecular analysis of Burkholderia cepacia complex isolates among cystic fibrosis patients at a referral center for lung transplantation. J Clin Microbiol 40:1188–1193

    Article  PubMed  CAS  Google Scholar 

  29. Golini G, Cazzola G, Fontana R (2006) Molecular epidemiology and antibiotic susceptibility of Burkholderia cepacia-complex isolates from an Italian cystic fibrosis centre. Eur J Clin Microbiol Infect Dis 25:175–180

    Article  PubMed  CAS  Google Scholar 

  30. Allice T, Scutera S, Chirillo MG, Savoia D (2006) Burkholderia respiratory tract infections in Italian patients with cystic fibrosis: molecular characterization. J Infect 53:159–165

    Article  PubMed  CAS  Google Scholar 

  31. Saiman L, Siegel J (2004) Infection control in cystic fibrosis. Clin Microbiol Rev 17:57–71

    Article  PubMed  Google Scholar 

  32. Valderrey AD, Pozuelo MJ, Jiménez PA, Maciá MD, Oliver A, Rotger R (2010) Chronic colonization by Pseudomonas aeruginosa of patients with obstructive lung diseases: cystic fibrosis, bronchiectasis, and chronic obstructive pulmonary disease. Diagn Microbiol Infect Dis 68:20–27

    Article  PubMed  Google Scholar 

  33. Kutty PK, Moody B, Gullion JS, Zervos M, Ajluni M, Washburn R, Sanderson R, Kainer MA, Powell TA, Clarke CF, Powell RJ, Pascoe N, Shams A, Lipuma JJ, Jensen B, Noble-Wang J, Arduino MJ, McDonald LC (2007) Multistate outbreak of Burkholderia cenocepacia colonization and infection associated with the use of intrinsically contaminated alcohol-free mouthwash. Chest 132:1825–1831

    Article  PubMed  Google Scholar 

  34. Nasser RM, Rahi AC, Haddad MF, Daoud Z, Irani-Hakime N, Almawi WY (2004) Outbreak of Burkholderia cepacia bacteremia traced to contaminated hospital water used for dilution of an alcohol skin antiseptic. Infect Control Hosp Epidemiol 25:231–239

    Article  PubMed  Google Scholar 

  35. Souza AV, Moreira CR, Pasternak J, Hirata Mde L, Saltini DA, Caetano VC, Ciosak S, Azevedo FM, Severino P, Vandamme P, Magalhães VD (2004) Characterizing uncommon Burkholderia cepacia complex isolates from an outbreak in a haemodialysis unit. J Med Microbiol 53:999–1005

    Article  PubMed  CAS  Google Scholar 

  36. Graindorge A, Menard A, Neto M, Bouvet C, Miollan R, Gaillard S, de Montclos H, Laurent F, Cournoyer B (2010) Epidemiology and molecular characterization of a clone of Burkholderia cenocepacia responsible for nosocomial pulmonary tract infections in a French intensive care unit. Diagn Microbiol Infect Dis 66:29–40

    Article  PubMed  CAS  Google Scholar 

  37. Jacobson M, Wray R, Kovach D, Henry D, Speert D, Matlow A (2006) Sustained endemicity of Burkholderia cepacia complex in a pediatric institution, associated with contaminated ultrasound gel. Infect Control Hosp Epidemiol 27:362–366

    Article  PubMed  Google Scholar 

  38. Messi P, Guerrieri E, Bondi M (2005) Antibiotic resistance and antibacterial activity in heterotrophic bacteria of mineral water origin. Sci Total Environ 346:213–219

    Article  PubMed  CAS  Google Scholar 

  39. Oie S, Matsuzaka Y, Kiyonaga H, Maeda K, Kamiya A (2008) Microbiological safety of bottled mineral water in patients susceptible to infections. Shokuhin Eiseigaku Zasshi 49:308–310

    Article  PubMed  Google Scholar 

  40. Jassem AN, Zlosnik JEA, Henry DA, Hancock REW, Ernst RK, Speert DP (2011) In vitro susceptibility of Burkholderia vietnamiensis to aminoglycosides. Antimicrob Agents Chemother 55:2256–2264

    Article  PubMed  CAS  Google Scholar 

  41. Vermis K, Vandamme PA, Nelis HJ (2003) Burkholderia cepacia complex genomovars: utilization of carbon sources, susceptibility to antimicrobial agents and growth on selective media. J Appl Microbiol 95:1191–1199

    Article  PubMed  CAS  Google Scholar 

  42. Bevivino A, Dalmastri C, Tabacchioni S, Chiarini L, Belli ML, Piana S, Materazzo A, Vandamme P, Manno G (2002) Burkholderia cepacia complex bacteria from clinical and environmental sources in Italy: genomovar status and distribution of traits related to virulence and transmissibility. J Clin Microbiol 40:846–851

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank the clinical microbiologists involved in the isolation and submission of Bcc strains to the Taxonomy Laboratory at the National Center for Microbiology (CNM).

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The authors declare that they have no conflict of interest.

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Correspondence to J. A. Saéz-Nieto.

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Medina-Pascual, M.J., Valdezate, S., Villalón, P. et al. Identification, molecular characterisation and antimicrobial susceptibility of genomovars of the Burkholderia cepacia complex in Spain. Eur J Clin Microbiol Infect Dis 31, 3385–3396 (2012). https://doi.org/10.1007/s10096-012-1707-6

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