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Journal of Clinical Microbiology, May 2000, p. 1763-1766, Vol. 38, No. 5
Laboratory of Hospital Infection, Central
Public Health Laboratory, London NW9 5HT, United Kingdom
Received 10 November 1999/Returned for modification 9 January
2000/Accepted 15 February 2000
In the last 15 years, Burkholderia cepacia has emerged
as a significant pathogen in cystic fibrosis (CF) patients, mainly due
to the severity of infection observed in a subset of patients and the
fear of transmission of the organism to noncolonized patients. Although
patients who deteriorate rapidly cannot be predicted by microbiological
characteristics, three genetic markers have been described for strains
that spread between patients. These are the cblA gene,
encoding giant cable pili; a hybrid of two insertion sequences,
IS1356 and IS402; and a 1.4-kb open reading frame known as the B. cepacia epidemic strain marker
(BCESM). The latter two are of unknown function. An epidemic strain
lineage was previously identified among CF patients in the United
Kingdom that apparently had spread from North America and that was
characterized by a specific random amplified polymorphic DNA (RAPD)
pattern. We searched for the described genetic markers using specific
PCR assays with 117 patient isolates of B. cepacia from 40 United Kingdom hospitals. Isolates were grouped according to genomovar and epidemic strain lineage RAPD pattern with a 10-base primer, P272. A
total of 41 isolates from patients in 12 hospitals were classified as
the epidemic strain, and 40 of these were distributed in genomovars
IIIa (11 isolates), IIIb (1 isolate), and IIIc (28 isolates). All
isolates of the epidemic strain were positive for the cblA
gene and BCESM, but two lacked the insertion sequence hybrid. None of
the 76 sporadic isolates contained cblA or the insertion
sequence hybrid, but 11 of them were positive for BCESM. Nonepidemic
isolates were distributed among genomovars I or IV (9), II (49), IIIa
(11), IIIb (3), and IIIc (4). There were three clusters of
cross-infection (one involving two patients and two involving three
patients) with isolates of genomovar II. We conclude that in the United
Kingdom, a single clonal lineage has spread between and within some
hospitals providing care for CF patients. The presence of the
cblA gene is the most specific marker for the epidemic
strain. We recommend that all isolates of B. cepacia from
CF patients should be screened by PCR to influence segregation and
infection control strategies.
The acquisition of
Burkholderia cepacia in the lungs of cystic fibrosis (CF)
patients is viewed with great concern. The reason is that 20 to 30% of
patients who become colonized with B. cepacia experience a
rapidly fatal necrotizing pneumonia with septicemia (the "cepacia
syndrome") (3). Cross-infection between patients with the
organism has been documented both in and out of the hospital (2). A single strain which had originally spread between
clinics in Edinburgh and Manchester during the late 1980s was
recognized as the predominant strain in many regional centers in the
United Kingdom and was found in about one-third of all patients
colonized with B. cepacia (9). This strain was
representative of the original North American clone, designated ET 12 (4).
Since the transfer of B. cepacia to the genus
Burkholderia, of which it is the type species
(16), the phenotypic and genotypic definitions of B. cepacia have received increasing attention. It is now widely
accepted that, rather than being a single species, B. cepacia is a complex of closely related species (11, 14, 15). According to the scheme of Vandamme et al. (14)
that described five genomovars of B. cepacia,
transmissible strains from CF patients fall mainly into genomovar III,
although recent French experience suggests that three of their
highly transmissible strains share characteristics with more than one
genomovar (11).
Various markers have been associated with transmissible strains of
B. cepacia. Giant fibers, known as cable pili, are found on
the surfaces of some isolates of B. cepacia, and these
fibers mediate adherence to respiratory mucins (10). The
genetic relatedness of isolates expressing cable pili from outbreaks in
CF patients suggested that this property was linked to the epidemic
spread of strains (12). A hybrid of two insertion sequences
(IS), IS402 and IS1356, was also found to be
exclusive to epidemic strains from Ontario, Canada, and the United
Kingdom (13); recently, a conserved 1.4-kb open
reading frame was identified in strains of B. cepacia
recovered from incidents of cross-infection between CF patients but was
absent from sporadic strains (6). The open reading frame
showed homology with a family of negative transcriptional regulatory
genes and was termed the B. cepacia epidemic strain marker
(BCESM). Transmissible strains also correlated with specific random
amplified polymorphic DNA (RAPD) patterns (5). However, none
of these factors has been positively associated with invasive strains,
and patients who succumb to cepacia syndrome cannot yet be predicted.
Current guidelines from the CF associations in both the United Kingdom
and the United States advise patients colonized with B. cepacia to avoid contact in confined areas with other patients to
reduce the risk of cross-infection. This has led to the segregation of
colonized from noncolonized patients, with its attendant psychosocial impact. The differentiation of transmissible from sporadic strains may
therefore have a role in infection control in this patient group by
identifying patients least likely to transmit infection to others. We
set out to determine the frequency of genes for the three markers
(cable pili, IS hybrid, and BCESM) in a collection of B. cepacia strains from CF patients and examined their association with the classification of a strain as epidemic or sporadic by epidemiological origin, RAPD pattern, and genomovar.
Bacterial isolates.
One hundred seventeen sputum isolates of
B. cepacia from 114 CF and 3 non-CF patients in 40 hospitals
in the United Kingdom were examined. Control strains included the index
Edinburgh epidemic strain (CF 5610), which was a gift from J. R. W. Govan, University of Edinburgh Medical School, Edinburgh,
United Kingdom, and reference strain NCTC 10661. Isolates were
confirmed as B. cepacia by PCR with specific 16S rRNA
primers as previously described (1). All isolates were
tested in the API 20NE gallery (bioMérieux, Basingstoke,
United Kingdom) and examined for Gram stain reaction; motility;
hydrolysis of casein, gelatin, starch, tyrosine, Tween 20, and Tween
80; production of DNase, catalase, oxidase, nitrate reductase,
and lecithinase; growth on MacConkey agar and B. cepacia selective agar (Mast, Bootle, United Kingdom); acid
production from ammonium salt sugars; and growth at 42°C. Isolates
were allocated to a genomovar on the basis of reactions in selected
tests (14).
Detection of genes for transmissibility factors.
The
oligonucleotide primers (Cruachem Ltd., Glasgow, United Kingdom) for
the amplification of genes encoding transmissibility factors are shown
in Table 1. Bacterial DNA was prepared by
emulsifying five colonies of 48-h growth from nutrient agar into 100 µl of sterile tissue culture water (Sigma, Dorset, United Kingdom). The DNA was denatured in a Dri-block (Techne, Duxford, United Kingdom)
at 100°C for 5 min, vortexed, and centrifuged at 13,000 × g for 5 min, and 3 µl of the supernatant was added to 12 µl of
water. A water blank (15 µl) was prepared. PCR was carried out with a
25-µl volume for each epidemic marker primer pair. This volume
contained 100 pmol of each primer, 50 pmol of MgCl2, 2.5 pmol of each deoxynucleotide triphosphate, 1.25 U of Taq DNA polymerase, and 2.5 µl of 10× PCR buffer (Life Technologies,
Paisley, United Kingdom). Amplification was carried out with a
GeneE thermal cycler (Techne). Products were separated in a
1.5% Nusieve agarose gel (Flowgen, Sittingbourne, United Kingdom) at
100 V for 1.5 h. Amplicon size was determined by comparison with a
123-bp ladder (Life Technologies).
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Copyright © 2000, American Society for Microbiology. All rights reserved.
Distribution of Genes Encoding Putative Transmissibility
Factors among Epidemic and Nonepidemic Strains of
Burkholderia cepacia from Cystic Fibrosis Patients in
the United Kingdom
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
TABLE 1.
Primers and conditions for PCR of transmissibility marker
genes of B. cepacia
RAPD profiling. Bacterial DNA for RAPD profiling was prepared by GES extraction (8), and 50 ng was added to 15 µl of sterile tissue culture water for PCR. The PCR reagents were as for the epidemic markers, except that 25 pmol of primer P272 (Table 1) was used. PCR was carried out with an Omnigene thermal cycler (Hybaid, Ashford, United Kingdom). Products were separated as described above, and profiles were compared with that of CF 5610.
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RESULTS |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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The control strain CF 5610 was positive for all three epidemic
markers by PCR, in contrast to NCTC 10661, which was negative for each
amplicon. Table 2 summarizes the results
for 117 clinical isolates identified as B. cepacia from 40 hospitals in the United Kingdom. Of these isolates, 41 were identified
as the same clone as strain CF 5610 by RAPD patterns and were isolated
from patients in 12 hospitals. Each of these isolates, except 1, was
classified in genomovar III
28 in IIIc (alkaline reaction in
oxidation-fermentation medium and negative reaction in ammonium salt
sugars), 11 in IIIa, and 1 in IIIb; the other isolate had a biochemical
profile indistinguishable from that described for B. gladioli (14). All 41 isolates were positive for
cblA and BCESM, and 39 were positive for the IS hybrid. Figure 1 illustrates the PCR assay
results for the three markers. The cblA amplicon gave a
clear strong band in all positive tests. Faint product bands were
visible in the lanes of some nonepidemic strains in the IS hybrid PCR,
although these were clearly distinguished from the specific product by
molecular size. Two distinct bands were obtained with BCESM primers on
most occasions, the lower-molecular-weight band corresponding to the
predicted product size.
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Of the 76 isolates with a RAPD profile distinct from that of CF 5610, none was positive for cblA or the IS hybrid, but 11 produced a product with the BCESM primers. More than half of these isolates were genomovar II (B. multivorans); 11 were genomovar IIIa, 3 were IIIb, 4 were IIIc, and 9 were I or IV. The 11 nonepidemic BCESM-positive isolates were randomly distributed among hospitals and genomovars, and all appeared to be unique.
There were three small clusters of cross-infection in three hospitals with genomovar II isolates and one hospital with a nonepidemic IIIa isolate. Two clusters involved three patients, and the other involved two patients. All of these isolates were BCESM negative, and none had the epidemic strain RAPD profile.
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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To minimize the risk of cross-infection, CF patients colonized with B. cepacia usually are treated on separate wards and attend different outpatient clinics than their noncolonized counterparts. They are also advised to avoid social contact with noncolonized patients. This is an emotive issue, as contact with other patients both in and out of the hospital is considered to be important for their general well-being. This fear is due mainly to the unpredictable course following acquisition of B. cepacia and the lack of knowledge of bacterial and host factors that influence clinical outcome. Evidence suggests that where segregation is practiced in hospitals, patients tend to acquire unique strains, whereas endemic strains predominate in hospitals with no segregation policy (7). Govan et al. showed that the main cause of an increase in B. cepacia colonization among CF patients in Edinburgh and Manchester in the late 1980s was an epidemic strain that had spread between centers (2). They also demonstrated that in one instance where a patient was infected with the epidemic strain and a second strain of B. cepacia, only the epidemic strain was passed on to another patient. Subsequently, the Edinburgh strain of B. cepacia was identified as being responsible for the colonization of approximately 30% of CF patients in 10 of 16 regional centers in the United Kingdom (9). It may therefore be of value for infection control purposes to identify patients colonized by strains with the potential to spread and to differentiate such patients from those harboring sporadic strains. Segregation of patients would thus be based on the properties of the strains rather than simply the presence or absence of the organism.
The description of putative transmissibility factors in CF-associated B. cepacia by North American workers prompted our investigation of the specificity of the factors among isolates from patients in the United Kingdom. We have shown here that the cblA gene is specific for and that the IS hybrid is indicative of strains of the epidemic lineage. These findings support the original findings that cblA and the hybrid of IS1356 inserted within IS402 were associated specifically with the North American epidemic strain lineage which subsequently emerged in Britain (12, 13). All but 2 of the 41 epidemic strains examined here contained the IS hybrid, a frequency almost identical to that reported previously by Tyler et al. for the North American clone (13). The IS hybrid may be linked to the apparent increase in transmissibility of the epidemic strain or may simply be a marker for this lineage. Mahenthiralingam et al. (5) identified a conserved region in RAPD profiles of seven strains of B. cepacia that had been associated with outbreaks of infection within groups of patients, and only one of these strains was cblA positive. They suggested that the presence of BCESM was related to the ability of a strain to spread between multiple patients. We identified BCESM in all isolates of the United Kingdom epidemic strain but also in 11 strains in all four genomovars of B. cepacia. These strains appeared to be unique, and there was no evidence of spread either within or between centers. We did, however, identify small clusters of cross-infection with strains that were BCESM negative.
The finding that all isolates, except one, of the epidemic strain were genomovar III was consistent with previous reports (14). However, Segonds et al. (11), using restriction fragment length polymorphism (RFLP) analysis of amplified 16S ribosomal DNA, found that three of five highly transmissible clones of B. cepacia in French CF centers belonged to a genomovar I- or III-related RFLP group. They also observed that one of the clones associated with fatal septicemia had a B. multivorans (genomovar II) RFLP pattern. It is noteworthy that more than half of the epidemic isolates described here, however, were genomovar IIIc, which is characterized by a loss of the ability to utilize all saccharide substrates. This feature could contribute to poor identification of asaccharolytic isolates and underlines the need for the confirmation of all biochemically atypical isolates by PCR with B. cepacia-specific primers (1, 15).
In conclusion, certain isolates of B. cepacia have a propensity for epidemic spread in the CF community; (i) these isolates are members of the same genomovar, (ii) they share a characteristic DNA fingerprint, and (iii) they possess a unique genetic marker that could have a profound affect on patient care. Patients colonized with transmissible strains may have to be segregated from patients colonized with sporadic strains, who themselves may not need to be segregated. In the United Kingdom, we have found only one clonal lineage of B. cepacia that has spread within and between hospitals. Almost all isolates of this strain possess genetic markers associated with transmissibility, the most specific of which is the presence of the cblA gene. We consider it necessary, therefore, for all isolates of B. cepacia recovered from CF patients to be tested for confirmation of species identity and transmissibility factors by PCR. The question remains as to whether patients colonized with epidemic strains are at greater or lesser risk of cepacia syndrome than those colonized with nonepidemic strains.
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FOOTNOTES |
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* Corresponding author. Mailing address: Laboratory of Hospital Infection, Central Public Health Laboratory, 61 Colindale Ave., London NW9 5HT, United Kingdom. Phone: 44 (0)208 200 4400. Fax: 44 (0)208 200 7449. E-mail: tpitt{at}phls.nhs.uk.
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REFERENCES |
|---|
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
|
|---|
| 1. | Clode, F. E., M. E. Kaufmann, H. Malnick, and T. L. Pitt. 1999. Evaluation of three oligonucleotide primer sets in PCR for the identification of Burkholderia cepacia and their differentiation from Burkholderia gladioli. J. Clin. Pathol. 52:173-176[Abstract]. |
| 2. | Govan, J. R. W., P. H. Brown, J. Maddison, C. J. Doherty, J. W. Nelson, M. Dodd, A. P. Greening, and A. K. Webb. 1993. Evidence for transmission of Pseudomonas cepacia by social contact in cystic fibrosis. Lancet 342:15-19[CrossRef][Medline]. |
| 3. | Govan, J. R. W., and J. W. Nelson. 1993. Microbiology of cystic fibrosis lung infections: themes and issues. J. R. Soc. Med. 86(Suppl. 20):11-18. |
| 4. |
Johnson, W. M.,
S. D. Tyler, and K. R. Rozee.
1994.
Linkage analysis of geographic and clinical clusters in Pseudomonas cepacia infections by multilocus enzyme electrophoresis and ribotyping.
J. Clin. Microbiol.
31:924-930 |
| 5. | Mahenthiralingam, E., M. E. Campbell, D. A. Henry, and D. P. Speert. 1996. Epidemiology of Burkholderia cepacia infection in patients with cystic fibrosis: analysis by randomly amplified polymorphic DNA fingerprinting. J. Clin. Microbiol. 34:2914-2920[Abstract]. |
| 6. | Mahenthiralingam, E., D. A. Simpson, and D. P. Speert. 1997. Identification and characterization of a novel DNA marker associated with epidemic Burkholderia cepacia strains recovered from patients with cystic fibrosis. J. Clin. Microbiol. 35:808-816[Abstract]. |
| 7. | Paul, M., M. Pegler, and R. Benn. 1998. Molecular epidemiology of Burkholderia cepacia in two Australian cystic fibrosis centres. J. Hosp. Infect. 38:19-26[CrossRef][Medline]. |
| 8. | Pitcher, D., N. Saunders, and R. Owen. 1989. Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett. Appl. Microbiol. 8:151-156. |
| 9. |
Pitt, T. L.,
M. E. Kaufmann,
P. S. Patel,
L. C. A. Benge,
S. Gaskin, and D. M. Livermore.
1996.
Type characterisation and antibiotic susceptibility of Burkholderia (Pseudomonas) cepacia isolates from patients with cystic fibrosis in the United Kingdom and the Republic of Ireland.
J. Med. Microbiol.
44:203-210 |
| 10. |
Sajjan, U. S.,
L. Sun,
R. Goldstein, and J. F. Forstner.
1995.
Cable (Cbl) type II pili of cystic fibrosis-associated Burkholderia (Pseudomonas) cepacia: nucleotide sequence of the cblA major subunit pilin gene and novel morphology of the assembled appendage fibers.
J. Bacteriol.
177:1030-1038 |
| 11. |
Segonds, C.,
T. Heulin,
N. Marty, and G. Chabanon.
1999.
Differentiation of Burkholderia species by PCR-restriction fragment length polymorphism analysis of the 16S rRNA gene and application to cystic fibrosis isolates.
J. Clin. Microbiol.
37:2201-2208 |
| 12. | Sun, L., R.-Z. Jiang, S. Steinbach, A. Holmes, C. Campanelli, J. Forstner, U. Sajjan, Y. Tan, M. Riley, and R. Goldstein. 1995. The emergence of a highly transmissible lineage of cbl+ Pseudomonas (Burkholderia) cepacia causing CF centre epidemics in North America and Britain. Nat. Med. 1:661-666[CrossRef][Medline]. |
| 13. | Tyler, S. D., K. R. Rozee, and W. M. Johnson. 1996. Identification of IS1356, a new insertion sequence, and its association with IS402 in epidemic strains of Burkholderia cepacia infecting cystic fibrosis patients. J. Clin. Microbiol. 34:1610-1616[Abstract]. |
| 14. |
Vandamme, P.,
B. Holmes,
M. VanCanneyt,
T. Coenye,
B. Hoste,
R. Coopman,
H. Revets,
S. Lauwers,
M. Gillis,
K. Kersters, and J. R. W. Govan.
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 |
| 15. |
van Pelt, C.,
C. M. Verduin,
W. H. F. Goessens,
M. C. Vos,
B. Tummler,
C. Segonds,
F. Reubsaet,
H. Verbrugh, and A. van Belkum.
1999.
Identification of Burkholderia spp. in the clinical microbiology laboratory: comparison of conventional and molecular methods.
J. Clin. Microbiol.
37:2158-2164 |
| 16. | Yabuuchi, E., Y. Kosaka, H. Oyaizu, I. Kano, H. Hotta, Y. Hashimoto, T. Ekazi, and M. Arakawa. 1992. Proposal of Burkholderia gen. nov. and transfer of seven species of the genus Pseudomonas homology group II to the new genus with the type species Burkholderia cepacia (Palleroni and Holmes 1981) comb. nov. Microbiol. Immunol. 36:1251-1275[Medline]. |
Journal of Clinical Microbiology, May 2000, p. 1763-1766, Vol. 38, No. 5
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Copyright © 2000, American Society for Microbiology. All rights reserved.
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Lutter, E., Lewenza, S., Dennis, J. J., Visser, M. B., Sokol, P. A.
(2001). Distribution of Quorum-Sensing Genes in the Burkholderia cepacia Complex. Infect. Immun.
69: 4661-4666
[Abstract] [Full Text] -
LiPUMA, J. J., SPILKER, T., GILL, L. H., CAMPBELL, P. W. III, LIU, L., MAHENTHIRALINGAM, E.
(2001). Disproportionate Distribution of Burkholderia cepacia Complex Species and Transmissibility Markers in Cystic Fibrosis. Am. J. Respir. Crit. Care Med.
164: 92-96
[Abstract] [Full Text] -
Henry, D. A., Mahenthiralingam, E., Vandamme, P., Coenye, T., Speert, D. P.
(2001). Phenotypic Methods for Determining Genomovar Status of the Burkholderia cepacia Complex. J. Clin. Microbiol.
39: 1073-1078
[Abstract] [Full Text]
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