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Several distinct species (genomovars) comprise bacteria previously identified merely as Burkholderia cepacia. Understanding how these species, collectively referred to as the B. cepacia complex, differ in their epidemiology and pathogenic potential in cystic fibrosis (CF) is important in efforts to refine management strategies. B. cepacia isolates recovered from 606 CF patients receiving care at 132 treatment centers in 105 cities in the United States were assessed to determine species within the B. cepacia complex and examined for the presence of putative transmissibility markers (B. cepacia epidemic strain marker [BCESM] and cable pilin subunit gene [cblA]). Fifty percent of patients were infected with B. cepacia complex genomovar III, 38% with B. multivorans (formerly genomovar II), and 5% with B. vietnamiensis (formerly genomovar V); fewer than 5% of patients were infected with either genomovar I, B. stabilis (formerly genomovar IV), genomovar VI, or genomovar VII. BCESM was found in 46% of genomovar III isolates and not in any other species. Only one isolate, from a patient infected with the ET12 epidemic lineage, contained the complete cblA pilin subunit gene. Our data indicate a differential capacity for human infection among the phylogenetically closely related species of the B. cepacia complex. The low frequency of BCESM and cblA suggests that they are not sufficient markers of B. cepacia virulence or transmissibility.
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The phytopathogenic bacterium Burkholderia cepacia has been recognized as an important opportunistic pathogen among persons with cystic fibrosis (CF) since the early 1980s (1, 2). In CF, pulmonary infection with B. cepacia is generally chronic, refractory to antimicrobial therapy, and associated with increased rates of morbidity and mortality. In fact, a significant proportion of patients with CF succumb to a rapidly progressive necrotizing pneumonia after acquisition of B. cepacia, and poor outcome in lung transplant recipients has led many centers to consider B. cepacia infection an absolute contraindication to transplantation. However, many CF patients remain colonized with B. cepacia for years without an apparent adverse impact on clinical course. Still others may be only transiently colonized. These differences in outcome suggest important differences in the epidemiology and pathogenic potential among B. cepacia strains or variability in critical host factors that have yet to be defined. A better understanding of these issues is needed to optimize current preventive and management strategies.
Recent comprehensive taxonomic analyses have defined several distinct yet closely related species among bacteria previously identified merely as B. cepacia based on phenotype alone (3). By convention, these newly described species are referred to as "genomovars" until distinguishing phenotypic features are identified that allow the proposal of formal binomial designations. Among the five species (genomovars I-V) initially identified, genomovar II has been renamed B. multivorans, while genomovar V was identified as the previously recognized species B. vietnamiensis (4). More recently, genomovar IV was renamed B. stabilis (5). The remaining two species continue to be referred to as B. cepacia complex genomovar I and genomovar III pending identification of differential phenotypes. Within the past year, analysis of bacteria recovered from clinical and environmental sources has identified two more species (genomovars VI and VII) that are also members of the B. cepacia complex (6, 7). The name Burkholderia ambifaria will be proposed for genomovar VII.
Although much remains unknown about the epidemiology of B. cepacia complex infection in CF, it is clear that interpatient transmission of certain strains can occur (8, 9). So-called epidemic strains predominate among patients in some centers and may have an enhanced capacity for spread (10, 11). The factors contributing to this are unknown, but putative transmissibility markers have been identified. The B. cepacia epidemic strain marker (BCESM), a 1.4-kb sequence containing an open reading frame (ORF) with homology to transcriptional regulatory genes, was found in several epidemic strains but was absent from unique strains for which there was no evidence of patient-to-patient spread (11). The cblA gene encodes the pilin subunit protein of so-called cable pili that mediate bacterial adherence to respiratory mucins (12). Cable pili are expressed by the B. cepacia ET12 clonal lineage, a genomovar III strain that predominates in Ontario, Canada, and is found in approximately one-third of all B. cepacia-colonized patients in the United Kingdom (13).
Because antimicrobial therapy is generally ineffective in eradicating B. cepacia complex infection, prevention of acquisition is an important goal of patient management. Stringent infection control policies that segregate colonized patients place a heavy economic and psychosocial burden on the CF community. A recent report recommends relaxation of infection control measures in the United Kingdom by requiring strict segregation only for patients colonized with transmissibility marker-positive genomovar III B. cepacia (14). However, it is not clear how broadly such a recommendation should be applied until a more complete picture is available of the distribution of B. cepacia complex species and putative transmissibility factors in CF. Systematic assessments of this distribution have not been performed and are complicated by difficulties inherent in accurate identification of B. cepacia complex bacteria (15). In this report we describe an analysis of B. cepacia complex recovered from over 600 colonized CF patients. The results indicate a highly disproportionate representation of species. The presence of either the BCESM or cblA may not be sufficient markers of virulence or transmissibility.
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Bacterial Isolates and Study Population
Since spring 1997 the Burkholderia cepacia Research Laboratory and Repository has received more than 2,400 putative B. cepacia isolates and related species for analysis. From among these we have identified 606 CF patients from whom B. cepacia has been recovered in sputum culture. These patients received care in 132 treatment centers in 105 cities in the United States, and all were registered in the Cystic Fibrosis Foundation Patient Registry (Bethesda, MD). For patients from whom multiple isolates were received, only the first to be confirmed as B. cepacia complex was included in the study.
Species Identification and Phylogenetic Analysis
All isolates were confirmed as B. cepacia complex by polyphasic analyses employing biochemical tests and genus- and species-specific 16S ribosomal ribonucleic acid (rRNA) polymerase chain reaction (PCR) as previously described (15). Differentiation of genomovars I, III and B. stabilis was made by using recA-targeted PCR as described (16). For isolates in which species identification remained equivocal after PCR testing, complete recA nucleotide sequences were obtained by using an ABI PRISM model 377XL DNA sequencer (Perkin-Elmer Applied Biosystems, Foster City, CA). Nucleotide sequences were manually checked and edited using Chromas software (Technelysium Pty Ltd; http://www.technelysium. com.http://au/chromas.html). Multiple alignments using the Clustal V method were performed among these sequences and 74 additional B. cepacia recA gene sequences (16). Phylogenetic trees were drawn by using DNASTAR software (MegAlign; DNASTAR, Inc., Madison, WI), and evolutionary relationships between recA genes were further determined by using the genetic distance-based neighbor-joining algorithms of the Data Analysis in Molecular Biology software (DAMBE; http://web. hku.hk/~xxia/http://software/software.htm) as described (16).
Detection of Putative Transmissibility Markers
The presence of the BCESM was detected by PCR with primers ESM-R1F (5'-GACAACGAGCAACGCGTAA-3') and ESM-R2R (5'GGCTCATCTGCGTATCGA3') which are specific for the internal 834 base pair (bp) ORF, esmR, described previously (11). In brief, bacterial DNA was prepared from colonies after 48 h growth with the Easy-DNA Kit (Invitrogen, Carlsbad, CA). PCR was carried out in a 25-µl volume containing 10 mM Tris-HCl, 50 mM KCl, 0.1% Triton X-100, 1.5 mM MgCl2, 400 µM deoxyribonucleoside triphosphates (dNTPs), 0.6 µM of each primer, 1 unit of Taq DNA polymerase (Promega, Madison, WI), and 50 ng of template DNA. Amplification was performed using a PTC-100 programmable thermal controller (MJ-Research, Incline Village, NV) as follows: 95° C for 3 min, then 30 cycles of 1 min at 94° C, 1 min at 62° C, and 1 min at 72° C, with a final extension step at 72° C for 10 min. Products were separated on a 2% agarose gel and visualized with ultraviolet (UV) light. A reaction with no template DNA was used as negative control, and isolate AU0355, a BCESM- and cblA-positive isolate of the ET12 clonal lineage originally isolated from a patient with CF in Toronto was used as a positive control. B. cepacia ATCC 25416 (genomovar I, BCESM- and cblA-negative) (17) was used as another negative control.
Bacterial isolates with genomic DNA sequences homologous to cblA were identified by dot-blot hybridization. In brief, approximately 1 µg of DNA from each of the 606 isolates was denatured at 100° C for 10 min, chilled directly on ice, dotted onto positively charged nylon membranes, and cross-linked by baking at 120° C for 30 min. A digoxigenin-labeled probe (PCR DIG Probe Synthesis Kit; Roche Molecular Biochemicals, Mannheim, Germany) specific for cblA sequences was generated by a PCR that used primers and conditions previously described (12). Membranes were hybridized overnight at 60° C, washed at 68° C three times (10 min each) in 2× wash solution (DIG Wash and Block Buffer Set, Roche) and twice more (10 min each) in 0.5× wash solution. Positive samples were identified by using anti-digoxigenin-AP Fab fragments and nitroblue tetrazolium/bromo(chloro)indolylphosphate (NBT-BCIP) (Roche, Mannheim, Germany) according to the manufacturer's instructions. DNA prepared from strain AU0355 was used as the positive control; ATCC 25416 again served as a negative control.
cblA Sequence Analysis
All isolates for which a positive signal for cblA sequences was obtained by dot-blot hybridization assay were further examined by cblA-specific PCR using primers and reaction conditions previously described (12). The nucleotide sequence of the resultant product from each isolate was determined as described earlier and analyzed using EditSeq and MegAlign sequence analysis software (DNASTAR).
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Species Identification and Phylogenetic Analysis
The distribution of species among the 606 B. cepacia complex isolates recovered from 606 CF patients is presented in Table 1. Fifty percent of patients were colonized with genomovar III; approximately 38% with B. multivorans; and 5% with B. vietnamiensis. Fewer than 5% of patients were colonized with either genomovar I, B. stabilis, genomovar VI, or genomovar VII. In 10 patients, the species of the colonizing isolate was indeterminate. For these isolates the B. cepacia complex species-specific rRNA and recA gene PCR assays were variable, but phylogenetic analysis using recA gene sequences clearly placed each within the B. cepacia complex (Figure 1). recA sequence cluster analysis also separated genomovar III isolates into two groups, III-A and III-B, as previously described (16). Among the 304 genomovar III isolates, 77 (25%) were Group III-A and 227 (75%) were Group III-B.
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Putative Transmissibility Markers and cblA Sequence Analysis
esmR, the internal ORF of the BCESM, was detected in 141 (46%) of the 304 genomovar III isolates. A greater proportion of Group III-A isolates were esmR-positive than were Group III-B (77% versus 36%, respectively). esmR sequences were not detected by PCR among any of the 302 isolates belonging to other (i.e., non-genomovar III) species.
Ten of the 606 isolates had DNA sequences with homology to cblA detected by dot-blot hybridization. Nine of these were genomovar I, whereas the remaining isolate was genomovar III (group III-A). Although DNA fragments of the predicted size were amplified from all 10 by cblA-specific PCR, only the product from the genomovar III isolate had 100% nucleotide sequence identity with the published ET12 cblA sequence (12) or the cblA sequence generated from AU0355. The genomovar III isolate was also BCESM-positive and macrorestriction genotype analysis by pulsed field gel electrophoresis demonstrated it to be of the ET12 lineage (data not shown). The cblA nucleotide sequences from the nine genomovar I isolates showed high identity (range, 98.1 to 100%) to each other, but lower identity (range 86.5 to 87.3%) to the published ET12 cblA sequence.
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The ability of B. cepacia to cause severe infection in, and spread among, persons with CF has led to the institution of stringent infection control measures that place a heavy burden on CF patients and their caregivers. A more complete understanding of B. cepacia epidemiology and pathology would allow the development of more effective and humane preventative strategies.
The recognition that several distinct species comprise bacteria formerly identified merely as "B. cepacia" provides a critical framework in this regard. In the initial description of the B. cepacia complex, Vandamme and colleagues identified CF sputum isolates belonging to each of five newly described species (3). However, this study included isolates from clinical and environmental sources and was not intended as a systematic survey of a defined CF population; as such, conclusions about the distribution of species in CF were limited. In the present study, we investigated B. cepacia recovered exclusively from clinical specimens and were careful to limit the study to only isolates from documented CF patients registered in the Cystic Fibrosis Foundation Patient Registry. We also took care to include only a single isolate from each patient in order to best assess the distribution of species in this population.
Our results reveal a highly disproportionate distribution of species with 88% of isolates belonging to either B. multivorans or genomovar III. As in the study by Vandamme and colleagues, we also identified CF isolates belonging to each species of the B. cepacia complex, including the newly described genomovars VI and VII. However, some species, such as B. stabilis, were rarely found. Thus, although all B. cepacia complex species described to date are capable of human infection, the distribution of species in CF indicates a differential capacity for pulmonary colonization or interpatient spread. The reasons for these differences among such phylogenetically closely related species are not known.
Nor is it yet clear whether these differences in relative frequency translate into significant differences in virulence, per se, between species. Observations from one CF center indicate increased rates of morbidity and mortality associated with genomovar III infection, suggesting that this species may be more problematic in CF than others (unpublished). The ET12 lineage, a genomovar III (recA Group III-A) strain that predominates in centers in eastern Canada and the United Kingdom, has been associated with "cepacia syndrome," but is also capable of chronic colonization with little apparent impact on clinical status. Thus, broad conclusions about the relative virulence of B. cepacia complex species are premature; patients with CF have succumbed with sepsis caused by B. multivorans (18). Whether species that are infrequently recovered in CF sputum (i.e., B. stabilis, B. vietnamiensis, and genomovars I, VI, and VII) have less capacity to cause severe disease has yet to be established.
How the distribution of species in CF compares with that among B. cepacia complex residing in the natural environment also requires elucidation. In striking contrast to the findings in CF patients, preliminary studies indicate that although all species can be found, genomovars I and VII seem to predominate in environmental samples (19). Additional study is underway to better define the biologic origins of strains infecting CF patients and the risks posed by strains likely to be encountered in the natural environment and those developed for commercial use as biocontrol and bioremediation agents.
By recA sequence-based phylogenetic analysis we identified several isolates that clearly clustered within the B. cepacia complex, but for which the precise species remains indeterminate at this time. These isolates would be identified as "B. cepacia" based on phenotype but gave variable reactions with 16S rRNA-specific and recA-specific PCR assays. Such strains may belong to phylogenetic subdivisions within currently defined genomovars (such as recA Groups III-A and III-B), or may represent other as yet undefined species belonging to the B. cepacia complex. Additional comprehensive taxonomic studies are necessary to more clearly define the breadth of species that may colonize the CF respiratory tract.
We and others have identified the presence in some CF centers of specific B. cepacia complex strains that are shared among several patients (10, 11, 20, 21). Such so-called epidemic or transmissible strains may have an enhanced ability to colonize or be spread among patients. The ET12 lineage, for example, spread between clinics in Toronto, Edinburgh, and Manchester in the late 1980s. Although detailed descriptions of other epidemic stains are lacking, there is a growing sense that most fall into genomovar III. However, multiple patients infected with the same B. multivorans strain have also been noted (18 and unpublished observations), and the "epidemic" strain involved in the first description of interpatient spread of B. cepacia is now known, in fact, to be genomovar VI (8, 22).
Methods to identify prospectively such epidemic or transmissible strains have been sought. Both cblA and the BCESM are features of ET12 (16). BCESM sequences were also identified in non-cblA-containing strains from several treatment centers in which there was evidence of patient-to-patient spread (11). Observations such as these have led some to recommend differential segregation policies for CF patients depending on the presence or absence of these putative transmissibility factors (14). In the present study, the BCESM (more specifically, esmR) was found exclusively in genomovar III strains. However, only 46% of genomovar III and 23% of 606 B. cepacia complex isolates overall were esmR-positive. A complete cblA gene was detected in only a single isolate. This was an ET12 strain recovered from a patient receiving care in Buffalo, New York, a city bordering Ontario, Canada, where the ET12 lineage predominates. (Interestingly, no other patient in this CF center was infected with ET12.) Several genomovar I isolates containing cblA homologues were also detected. Other non-genomovar III isolates containing sequences with homology to cblA have been identified, but in general these do not express cable pili-associated adhesin that mediates binding to respiratory epithelial cells (Umadevi S. Sajjan, personal communication).
Thus, although BCESM and cblA (in the case of the highly transmissible ET12 lineage) have been associated with epidemic strains, the great majority of B. cepacia complex- infected patients in this study harbored strains that were neither BCESM-positive nor cblA-positive. Additional isolate genotyping analyses are needed to determine more precisely the frequency of BCESM among strains in this collection for which there is evidence of interpatient spread. Preliminary analysis indicates that at least one major lineage, involving nearly all B. cepacia-colonized patients in two large CF centers, is both BCESM-negative and cblA-negative (unpublished).
In summary, although all species of the B. cepacia complex are capable of human infection, their disproportionate representation among CF patients implies critical differences in pathobiology. A fuller appreciation of these differences underlies the development of more effective strategies for prevention and, ultimately, therapy of B. cepacia complex infection in CF. However, broad adoption of recent efforts to stratify infection control measures based solely on infecting species or the presence of putative transmissibility factors would seem premature in light of our findings.
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Correspondence and requests for reprints should be addressed to Dr. John J. LiPuma, University of Michigan, 1150 W. Medical Center Drive, 8323 MSRB III, Box 0646, Ann Arbor, MI 48109-0646. E-mail: jlipuma{at}umich.edu
(Received in original form November 30, 2000 and in revised form March 7, 2001).
Acknowledgments: The authors thank Monica Brooks, Ase Sewell, Theresa Zaccone, Liliana Fresneda, and Julie Fadden for excellent technical assistance. We also gratefully acknowledge the generosity and cooperation of participating CF centers and microbiology laboratories for submission of clinical isolates.
Supported by grants from the Cystic Fibrosis Foundation ( J.J.L.) and the Cystic Fibrosis Trust (E.M., Grant PJ472).
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References |
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1. Isles A, Maclusky I, Corey M, Gold R, Prober C, Fleming P, Levison H. Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J Pediatr 1984; 104: 206-210 [Medline].
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L. Jorda-Vargas, N. C. Castaneda, D. Centron, J. Degrossi, M. D'Aquino, M. A. Valvano, A. Procopio, and L. Galanternik Prevalence of Indeterminate Genetic Species of Burkholderia cepacia Complex in a Cystic Fibrosis Center in Argentina J. Clin. Microbiol., March 1, 2008; 46(3): 1151 - 1152. [Full Text] [PDF]
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 K. D. Seed and J. J. Dennis Development of Galleria mellonella as an Alternative Infection Model for the Burkholderia cepacia Complex Infect. Immun., March 1, 2008; 76(3): 1267 - 1275. [Abstract] [Full Text] [PDF]
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S. P. Bernier, D. T. Nguyen, and P. A. Sokol A LysR-Type Transcriptional Regulator in Burkholderia cenocepacia Influences Colony Morphology and Virulence Infect. Immun., January 1, 2008; 76(1): 38 - 47. [Abstract] [Full Text] [PDF]
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A. Baldwin, E. Mahenthiralingam, P. Drevinek, C. Pope, D. J. Waine, D. A. Henry, D. P. Speert, P. Carter, P. Vandamme, J. J. LiPuma, et al. Elucidating Global Epidemiology of Burkholderia multivorans in Cases of Cystic Fibrosis by Multilocus Sequence Typing J. Clin. Microbiol., January 1, 2008; 46(1): 290 - 295. [Abstract] [Full Text] [PDF]
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 E. M. Caraher, K. Gumulapurapu, C. C. Taggart, P. Murphy, S. McClean, and M. Callaghan The effect of recombinant human lactoferrin on growth and the antibiotic susceptibility of the cystic fibrosis pathogen Burkholderia cepacia complex when cultured planktonically or as biofilms J. Antimicrob. Chemother., September 1, 2007; 60(3): 546 - 554. [Abstract] [Full Text] [PDF]
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M. V. Cunha, A. Pinto-de-Oliveira, L. Meirinhos-Soares, M. J. Salgado, J. Melo-Cristino, S. Correia, C. Barreto, and I. Sa-Correia Exceptionally High Representation of Burkholderia cepacia among B. cepacia Complex Isolates Recovered from the Major Portuguese Cystic Fibrosis Center J. Clin. Microbiol., May 1, 2007; 45(5): 1628 - 1633. [Abstract] [Full Text] [PDF]
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 R. J. Malott and P. A. Sokol Expression of the bviIR and cepIR Quorum-Sensing Systems of Burkholderia vietnamiensis J. Bacteriol., April 15, 2007; 189(8): 3006 - 3016. [Abstract] [Full Text] [PDF]
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C. H Goss and J. L Burns Exacerbations in cystic fibrosis {middle dot} 1: Epidemiology and pathogenesis Thorax, April 1, 2007; 62(4): 360 - 367. [Abstract] [Full Text] [PDF]
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C. Kooi, B. Subsin, R. Chen, B. Pohorelic, and P. A. Sokol Burkholderia cenocepacia ZmpB Is a Broad-Specificity Zinc Metalloprotease Involved in Virulence Infect. Immun., July 1, 2006; 74(7): 4083 - 4093. [Abstract] [Full Text] [PDF]
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 J S Elborn Practical Management of Cystic Fibrosis Chronic Respiratory Disease, July 1, 2006; 3(3): 161 - 165. [PDF]
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R.-P. Vonberg, S. Haussler, P. Vandamme, and I. Steinmetz Identification of Burkholderia cepacia complex pathogens by rapid-cycle PCR with fluorescent hybridization probes J. Med. Microbiol., June 1, 2006; 55(6): 721 - 727. [Abstract] [Full Text] [PDF]
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 L. A. Kalish, D. A. Waltz, M. Dovey, G. Potter-Bynoe, A. J. McAdam, J. J. LiPuma, C. Gerard, and D. Goldmann Impact of Burkholderia dolosa on Lung Function and Survival in Cystic Fibrosis Am. J. Respir. Crit. Care Med., February 15, 2006; 173(4): 421 - 425. [Abstract] [Full Text] [PDF]
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D. T. Kenna, H. Yesilkaya, K. J. Forbes, V. A. Barcus, P. Vandamme, and J. R. W. Govan Distribution and genomic location of active insertion sequences in the Burkholderia cepacia complex J. Med. Microbiol., January 1, 2006; 55(1): 1 - 10. [Abstract] [Full Text] [PDF]
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P. W. Whitby, T. M. VanWagoner, A. A. Taylor, T. W. Seale, D. J. Morton, J. J. LiPuma, and T. L. Stull Identification of an RTX determinant of Burkholderia cenocepacia J2315 by subtractive hybridization J. Med. Microbiol., January 1, 2006; 55(1): 11 - 21. [Abstract] [Full Text] [PDF]
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S. Gingues, C. Kooi, M. B. Visser, B. Subsin, and P. A. Sokol Distribution and Expression of the ZmpA Metalloprotease in the Burkholderia cepacia Complex J. Bacteriol., December 15, 2005; 187(24): 8247 - 8255. [Abstract] [Full Text] [PDF]
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J. Y. Kim, U. S. Sajjan, G. P. Krasan, and J. J. LiPuma Disruption of Tight Junctions during Traversal of the Respiratory Epithelium by Burkholderia cenocepacia Infect. Immun., November 1, 2005; 73(11): 7107 - 7112. [Abstract] [Full Text] [PDF]
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E Mahenthiralingam and P Vandamme Taxonomy and pathogenesis of the Burkholderia cepacia complex Chronic Respiratory Disease, October 1, 2005; 2(4): 209 - 217. [Abstract] [PDF]
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S. Campana, G. Taccetti, N. Ravenni, F. Favari, L. Cariani, A. Sciacca, D. Savoia, A. Collura, E. Fiscarelli, G. De Intinis, et al. Transmission of Burkholderia cepacia Complex: Evidence for New Epidemic Clones Infecting Cystic Fibrosis Patients in Italy J. Clin. Microbiol., October 1, 2005; 43(10): 5136 - 5142. [Abstract] [Full Text] [PDF]
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A. Baldwin, E. Mahenthiralingam, K. M. Thickett, D. Honeybourne, M. C. J. Maiden, J. R. Govan, D. P. Speert, J. J. LiPuma, P. Vandamme, and C. G. Dowson Multilocus Sequence Typing Scheme That Provides Both Species and Strain Differentiation for the Burkholderia cepacia Complex J. Clin. Microbiol., September 1, 2005; 43(9): 4665 - 4673. [Abstract] [Full Text] [PDF]
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R. J. Malott, A. Baldwin, E. Mahenthiralingam, and P. A. Sokol Characterization of the cciIR Quorum-Sensing System in Burkholderia cenocepacia Infect. Immun., August 1, 2005; 73(8): 4982 - 4992. [Abstract] [Full Text] [PDF]
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S. P. Bernier and P. A. Sokol Use of Suppression-Subtractive Hybridization To Identify Genes in the Burkholderia cepacia Complex That Are Unique to Burkholderia cenocepacia J. Bacteriol., August 1, 2005; 187(15): 5278 - 5291. [Abstract] [Full Text] [PDF]
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G. W. Payne, P. Vandamme, S. H. Morgan, J. J. LiPuma, T. Coenye, A. J. Weightman, T. H. Jones, and E. Mahenthiralingam Development of a recA Gene-Based Identification Approach for the Entire Burkholderia Genus Appl. Envir. Microbiol., July 1, 2005; 71(7): 3917 - 3927. [Abstract] [Full Text] [PDF]
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R. Reik, T. Spilker, and J. J. LiPuma Distribution of Burkholderia cepacia Complex Species among Isolates Recovered from Persons with or without Cystic Fibrosis J. Clin. Microbiol., June 1, 2005; 43(6): 2926 - 2928. [Abstract] [Full Text] [PDF]
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X. Ortega, T. A. Hunt, S. Loutet, A. D. Vinion-Dubiel, A. Datta, B. Choudhury, J. B. Goldberg, R. Carlson, and M. A. Valvano Reconstitution of O-Specific Lipopolysaccharide Expression in Burkholderia cenocepacia Strain J2315, Which Is Associated with Transmissible Infections in Patients with Cystic Fibrosis J. Bacteriol., February 15, 2005; 187(4): 1324 - 1333. [Abstract] [Full Text] [PDF]
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A. McDowell, S. Valanne, G. Ramage, M. M. Tunney, J. V. Glenn, G. C. McLorinan, A. Bhatia, J.-F. Maisonneuve, M. Lodes, D. H. Persing, et al. Propionibacterium acnes Types I and II Represent Phylogenetically Distinct Groups J. Clin. Microbiol., January 1, 2005; 43(1): 326 - 334. [Abstract] [Full Text] [PDF]
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A M Jones, M E Dodd, J R W Govan, V Barcus, C J Doherty, J Morris, and A K Webb Burkholderia cenocepacia and Burkholderia multivorans: influence on survival in cystic fibrosis Thorax, November 1, 2004; 59(11): 948 - 951. [Abstract] [Full Text] [PDF]
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S. Brisse, C. Cordevant, P. Vandamme, P. Bidet, C. Loukil, G. Chabanon, M. Lange, and E. Bingen Species Distribution and Ribotype Diversity of Burkholderia cepacia Complex Isolates from French Patients with Cystic Fibrosis J. Clin. Microbiol., October 1, 2004; 42(10): 4824 - 4827. [Abstract] [Full Text] [PDF]
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A. S. Engledow, E. G. Medrano, E. Mahenthiralingam, J. J. LiPuma, and C. F. Gonzalez Involvement of a Plasmid-Encoded Type IV Secretion System in the Plant Tissue Watersoaking Phenotype of Burkholderia cenocepacia J. Bacteriol., September 15, 2004; 186(18): 6015 - 6024. [Abstract] [Full Text] [PDF]
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A. D. Vinion-Dubiel, T. Spilker, C. R. Dean, H. Monteil, J. J. LiPuma, and J. B. Goldberg Correlation of wbiI Genotype, Serotype, and Isolate Source within Species of the Burkholderia cepacia Complex J. Clin. Microbiol., September 1, 2004; 42(9): 4121 - 4126. [Abstract] [Full Text] [PDF]
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U. Sajjan, S. Keshavjee, and J. Forstner Responses of Well-Differentiated Airway Epithelial Cell Cultures from Healthy Donors and Patients with Cystic Fibrosis to Burkholderia cenocepacia Infection Infect. Immun., July 1, 2004; 72(7): 4188 - 4199. [Abstract] [Full Text] [PDF]
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D. P. Speert and J. B. Goldberg Burkholderia cepacia Complex and Cystic Fibrosis: In Search of the Smoking Gun Am. J. Respir. Crit. Care Med., July 1, 2004; 170(1): 6 - 7. [Full Text] [PDF]
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A. McDowell, E. Mahenthiralingam, K. E.A. Dunbar, J. E. Moore, M. Crowe, and J. S. Elborn Epidemiology of Burkholderia cepacia complex species recovered from cystic fibrosis patients: issues related to patient segregation J. Med. Microbiol., July 1, 2004; 53(7): 663 - 668. [Abstract] [Full Text] [PDF]
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A. De Soyza, C. D. Ellis, C. M. A. Khan, P. A. Corris, and R. D. de Hormaeche Burkholderia cenocepacia Lipopolysaccharide, Lipid A, and Proinflammatory Activity Am. J. Respir. Crit. Care Med., July 1, 2004; 170(1): 70 - 77. [Abstract] [Full Text] [PDF]
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 K. De Boeck, A. Malfroot, L. Van Schil, P. Lebecque, C. Knoop, J.R.W. Govan, C. Doherty, S. Laevens, and P. Vandamme Epidemiology of Burkholderia cepacia complex colonisation in cystic fibrosis patients Eur. Respir. J., June 1, 2004; 23(6): 851 - 856. [Abstract] [Full Text] [PDF]
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 K. Vermis, T. Coenye, J. J. LiPuma, E. Mahenthiralingam, H. J. Nelis, and P. Vandamme Proposal to accommodate Burkholderia cepacia genomovar VI as Burkholderia dolosa sp. nov. Int J Syst Evol Microbiol, May 1, 2004; 54(3): 689 - 691. [Abstract] [Full Text] [PDF]
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M. Plesa, A. Kholti, K. Vermis, P. Vandamme, S. Panagea, C. Winstanley, and P. Cornelis Conservation of the opcL gene encoding the peptidoglycan-associated outer-membrane lipoprotein among representatives of the Burkholderia cepacia complex J. Med. Microbiol., May 1, 2004; 53(5): 389 - 398. [Abstract] [Full Text] [PDF]
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G. Manno, C. Dalmastri, S. Tabacchioni, P. Vandamme, R. Lorini, L. Minicucci, L. Romano, A. Giannattasio, L. Chiarini, and A. Bevivino Epidemiology and Clinical Course of Burkholderia cepacia Complex Infections, Particularly Those Caused by Different Burkholderia cenocepacia Strains, among Patients Attending an Italian Cystic Fibrosis Center J. Clin. Microbiol., April 1, 2004; 42(4): 1491 - 1497. [Abstract] [Full Text] [PDF]
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A. Baldwin, P. A. Sokol, J. Parkhill, and E. Mahenthiralingam The Burkholderia cepacia Epidemic Strain Marker Is Part of a Novel Genomic Island Encoding Both Virulence and Metabolism-Associated Genes in Burkholderia cenocepacia Infect. Immun., March 1, 2004; 72(3): 1537 - 1547. [Abstract] [Full Text] [PDF]
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 L. Saiman and J. Siegel Infection Control in Cystic Fibrosis Clin. Microbiol. Rev., January 1, 2004; 17(1): 57 - 71. [Abstract] [Full Text] [PDF]
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J. F. Turton, M. E. Kaufmann, N. Mustafa, S. Kawa, F. E. Clode, and T. L. Pitt Molecular Comparison of Isolates of Burkholderia multivorans from Patients with Cystic Fibrosis in the United Kingdom J. Clin. Microbiol., December 1, 2003; 41(12): 5750 - 5754. [Abstract] [Full Text] [PDF]
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P. A. Sokol, U. Sajjan, M. B. Visser, S. Gingues, J. Forstner, and C. Kooi The CepIR quorum-sensing system contributes to the virulence of Burkholderia cenocepacia respiratory infections Microbiology, December 1, 2003; 149(12): 3649 - 3658. [Abstract] [Full Text] [PDF]
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W. G. Veloira, P. Domenico, J. J. LiPuma, J. M. Davis, E. Gurzenda, and J. A. Kazzaz In vitro activity and synergy of bismuth thiols and tobramycin against Burkholderia cepacia complex J. Antimicrob. Chemother., December 1, 2003; 52(6): 915 - 919. [Abstract] [Full Text] [PDF]
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R. L. Gibson, J. L. Burns, and B. W. Ramsey Pathophysiology and Management of Pulmonary Infections in Cystic Fibrosis Am. J. Respir. Crit. Care Med., October 15, 2003; 168(8): 918 - 951. [Abstract] [Full Text] [PDF]
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S. P. Bernier, L. Silo-Suh, D. E. Woods, D. E. Ohman, and P. A. Sokol Comparative Analysis of Plant and Animal Models for Characterization of Burkholderia cepacia Virulence Infect. Immun., September 1, 2003; 71(9): 5306 - 5313. [Abstract] [Full Text] [PDF]
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M. V. Cunha, J. H. Leitao, E. Mahenthiralingam, P. Vandamme, L. Lito, C. Barreto, M. J. Salgado, and I. Sa-Correia Molecular Analysis of Burkholderia cepacia Complex Isolates from a Portuguese Cystic Fibrosis Center: a 7-Year Study J. Clin. Microbiol., September 1, 2003; 41(9): 4113 - 4120. [Abstract] [Full Text] [PDF]
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M. G. Detsika, J. E. Corkill, M. Magalhaes, K. J. Glendinning, C. A. Hart, and C. Winstanley Molecular Typing of, and Distribution of Genetic Markers among, Burkholderia cepacia Complex Isolates from Brazil J. Clin. Microbiol., September 1, 2003; 41(9): 4148 - 4153. [Abstract] [Full Text] [PDF]
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A. D. Vinion-Dubiel and J. B. Goldberg Review: Lipopolysaccharide of Burkholderia cepacia complex Innate Immunity, August 1, 2003; 9(4): 201 - 213. [Abstract] [PDF]
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C. R. Corbett, M. N. Burtnick, C. Kooi, D. E. Woods, and P. A. Sokol An extracellular zinc metalloprotease gene of Burkholderia cepacia Microbiology, August 1, 2003; 149(8): 2263 - 2271. [Abstract] [Full Text] [PDF]
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L. Liu, T. Spilker, T. Coenye, and J. J. LiPuma Identification by Subtractive Hybridization of a Novel Insertion Element Specific for Two Widespread Burkholderia cepacia Genomovar III Strains J. Clin. Microbiol., June 1, 2003; 41(6): 2471 - 2476. [Abstract] [Full Text] [PDF]
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R. Langley, D. T. Kenna, P. Vandamme, R. Ure, and J. R. W. Govan Lysogeny and bacteriophage host range within the Burkholderia cepacia complex J. Med. Microbiol., June 1, 2003; 52(6): 483 - 490. [Abstract] [Full Text] [PDF]
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T. Coenye and J. J. LiPuma Population structure analysis of Burkholderia cepacia genomovar III: varying degrees of genetic recombination characterize major clonal complexes Microbiology, January 1, 2003; 149(1): 77 - 88. [Abstract] [Full Text] [PDF]
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U. Sajjan, L. Liu, A. Lu, T. Spilker, J. Forstner, and J. J. LiPuma Lack of cable pili expression by cblA-containing Burkholderia cepacia complex Microbiology, November 1, 2002; 148(11): 3477 - 3484. [Abstract] [Full Text] [PDF]
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K. VERMIS, T. COENYE, E. MAHENTHIRALINGAM, H. J. NELIS, and P. VANDAMME Evaluation of species-specific recA-based PCR tests for genomovar level identification within the Burkholderia cepacia complex J. Med. Microbiol., November 1, 2002; 51(11): 937 - 940. [Abstract] [Full Text] [PDF]
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T. Coenye, T. Spilker, A. Martin, and J. J. LiPuma Comparative Assessment of Genotyping Methods for Epidemiologic Study of Burkholderia cepacia Genomovar III J. Clin. Microbiol., September 1, 2002; 40(9): 3300 - 3307. [Abstract] [Full Text] [PDF]
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P. Drevinek, H. Hrbackova, O. Cinek, J. Bartosova, O. Nyc, A. Nemec, and P. Pohunek Direct PCR Detection of Burkholderia cepacia Complex and Identification of Its Genomovars by Using Sputum as Source of DNA J. Clin. Microbiol., September 1, 2002; 40(9): 3485 - 3488. [Abstract] [Full Text] [PDF]
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S. Nzula, P. Vandamme, and J. R. W. Govan Influence of taxonomic status on the in vitro antimicrobial susceptibility of the Burkholderia cepacia complex J. Antimicrob. Chemother., August 1, 2002; 50(2): 265 - 269. [Abstract] [Full Text] [PDF]
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U. Schwab, M. Leigh, C. Ribeiro, J. Yankaskas, K. Burns, P. Gilligan, P. Sokol, and R. Boucher Patterns of Epithelial Cell Invasion by Different Species of the Burkholderia cepacia Complex in Well-Differentiated Human Airway Epithelia Infect. Immun., August 1, 2002; 70(8): 4547 - 4555. [Abstract] [Full Text] [PDF]
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E. MAHENTHIRALINGAM, A. BALDWIN, and P. VANDAMME Burkholderia cepacia complex infection in patients with cystic fibrosis J. Med. Microbiol., July 1, 2002; 51(7): 533 - 538. [Abstract] [Full Text] [PDF]
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S. Brisse, S. Stefani, J. Verhoef, A. Van Belkum, P. Vandamme, and W. Goessens Comparative Evaluation of the BD Phoenix and VITEK 2 Automated Instruments for Identification of Isolates of the Burkholderia cepacia Complex J. Clin. Microbiol., May 1, 2002; 40(5): 1743 - 1748. [Abstract] [Full Text] [PDF]
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D. G. Heath, K. Hohneker, C. Carriker, K. Smith, J. Routh, J. J. LiPuma, R. M. Aris, D. Weber, and P. H. Gilligan Six-Year Molecular Analysis of Burkholderia cepacia Complex Isolates among Cystic Fibrosis Patients at a Referral Center for Lung Transplantation J. Clin. Microbiol., April 1, 2002; 40(4): 1188 - 1193. [Abstract] [Full Text] [PDF]
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A. Bevivino, C. Dalmastri, S. Tabacchioni, L. Chiarini, M. L. Belli, S. Piana, A. Materazzo, P. Vandamme, and G. Manno 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., March 1, 2002; 40(3): 846 - 851. [Abstract] [Full Text] [PDF]
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M. J. TOBIN Pediatrics, Surfactant, and Cystic Fibrosis in AJRCCM 2001 Am. J. Respir. Crit. Care Med., March 1, 2002; 165(5): 619 - 630. [Full Text] [PDF]
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R. M. ARIS, J. C. ROUTH, J. J. LIPUMA, D. G. HEATH, and P. H. GILLIGAN Lung Transplantation for Cystic Fibrosis Patients with Burkholderia cepacia Complex . Survival Linked to Genomovar Type Am. J. Respir. Crit. Care Med., December 1, 2001; 164(11): 2102 - 2106. [Abstract] [Full Text] [PDF]
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T. Coenye, P. Vandamme, J. R. W. Govan, and J. J. LiPuma Taxonomy and Identification of the Burkholderia cepacia Complex J. Clin. Microbiol., October 1, 2001; 39(10): 3427 - 3436. [Full Text] [PDF]
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