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Epidemiology of Burkholderia Cepacia Complex in Patients with Cystic Fibrosis, Canada David P

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Epidemiology of Burkholderia Cepacia Complex in Patients with Cystic Fibrosis, Canada David P RESEARCH Epidemiology of Burkholderia cepacia Complex in Patients with Cystic Fibrosis, Canada David P. Speert,* Deborah Henry,* Peter Vandamme,† Mary Corey,‡ and Eshwar Mahenthiralingam* The Burkholderia cepacia complex is an important group of pathogens in patients with cystic fibrosis (CF). Although evidence for patient-to-patient spread is clear, microbial factors facilitating transmission are poorly understood. To identify microbial clones with enhanced transmissibility, we evaluated B. cepacia complex isolates from patients with CF from throughout Canada. A total of 905 isolates from the B. cepacia complex were recovered from 447 patients in 8 of the 10 provinces; 369 (83%) of these patients had genomovar III and 43 (9.6%) had B. multivorans (genomovar II). Infection prevalence differed substantially by region (22% of patients in Ontario vs. 5% in Quebec). Results of typing by random amplified polymor- phic DNA analysis or pulsed-field gel electrophoresis indicated that strains of B. cepacia complex from genomovar III are the most potentially transmissible and that the B. cepacia epidemic strain marker is a robust marker for transmissibility. urkholderia cepacia complex is an important group of and genomovar VII = B. ambifaria. Genomovars I and III can- B pathogens in immunocompromised hosts, notably those not be differentiated phenotypically, nor can B. multivorans with cystic fibrosis (CF) or chronic granulomatous disease and genomovar VI; these species must be distinguished by (1,2). Lung infections with B. cepacia complex in certain genetic methods. Bacteria from each of the genomovars have patients with CF result in rapidly progressive, invasive, fatal been recovered from patients with CF, but the predominant bacteremic disease (3). Furthermore, the bacteria have a poten- isolates in North America are from genomovar III and B. mul- tial for patient-to-patient spread, both within and outside the tivorans (12). hospital (4-9), raising questions about optimal measures for Numerous questions about the epidemiology of B. cepacia infection control. complex in CF are unanswered; for example, it is not known if The disease risk for infection with B. cepacia complex in certain genomovars or strains are more virulent than others. patients with CF is substantially higher than with Pseudomo- The relative risk for patient-to-patient spread of strains from nas aeruginosa alone or with bacteria other than B. cepacia or each of the different genomovars is also unknown. Two P. aeruginosa (10). However, there is a dramatic heterogeneity genetic elements have been identified in strains having a pro- in outcome among CF patients infected with B. cepacia com- pensity for epidemic spread. First, cblA, which encodes the plex: some patients have a fulminant decline in pulmonary protein for cable pilus production, is found in a single highly function, and others harbor B. cepacia complex for extended transmissible lineage from genomovar III that clusters among periods of time with no obvious adverse effects. The marked patients in the United Kingdom and Canada (13). Second, the difference in prognosis among infected patients has not been B. cepacia epidemic strain marker (BCESM), which encodes a adequately explained but is thought to result in part from dif- protein of unknown function, is found in many different strains ferences among infecting strains of B. cepacia complex. from genomovar III, each of which is clustered in specific CF B. cepacia is a genetically highly diverse class of bacteria, treatment centers (14). which is composed of several different species and discrete Infection with bacteria from the B. cepacia complex has a groups constituting the B. cepacia complex (11). Each group profound effect on the lives of patients with CF. Since B. cepa- differs sufficiently from the others to constitute a species, and cia complex infection can be spread from one CF patient to those that are phenotypically distinct have been assigned spe- another, provisions have been introduced in hospitals to limit cies designation. Those that cannot be differentiated phenotyp- contact among these patients. Infected patients are prohibited ically but are genetically distinct are defined as genomovars in some countries from attending social gatherings where other (11). As phenotypic differentiation among the genomovars has CF patients may be in attendance. Furthermore, since viru- improved over the past decade, new species designation has lence appears to differ among strains and one strain may been assigned as follows: genomovar II = B. multivorans, replace another, policies have been introduced in some centers genomovar IV = B. stabilis, genomovar V = B. vietnamiensis, to limit contact among patients who are infected with any strain from the B. cepacia complex. Lack of a clear under- *University of British Columbia and Children’s and Women’s Health standing about the epidemiology of B. cepacia complex and Centre of British Columbia, Vancouver, British Columbia, Canada; the relative risk of infection with each of the different genomo- †University of Ghent, Ghent, Belgium; and ‡The Hospital for Sick Chil- dren, Toronto, Ontario, Canada vars has spawned anxiety and confusion among CF patients, Emerging Infectious Diseases • Vol. 8, No. 2, February 2002 181 RESEARCH their caregivers, and families. Infection control policies have (PML Microbiologicals, Richmond, British Columbia, Can- been developed in an effort to balance the rights of CF patients ada). Bacteria were incubated for up to 7 days at 35°C in the with careful consideration of their physical and mental health. following sugars: glucose, maltose, lactose, xylose, sucrose, With burgeoning knowledge about the taxonomy, epidemi- and adonitol. Moeller lysine, ornithine, and negative control ology, and virulence of the B. cepacia complex, many ques- were also heavily inoculated and incubated at 35°C for 48 tions about appropriate infection control precautions have hours. The API 20 NE strip (Biomerieux Vitek Inc., Hazel- been raised. Consensus has been difficult to attain because of wood, MO) was set up according to manufacturer’s instruc- incomplete and conflicting data from various regions through- tions, except that the strip was incubated at 35°C and observed out the world. We undertook this study to provide a database at 24 and 48 hours. Growth on MacConkey agar without crys- from which infection control questions could begin to be tal violet (Difco Laboratories, Detroit, MI) and on B cepacia answered. selective agar (16) at 35°C was observed at 24 and 48 hours. In 1994 a B. cepacia complex research and referral reposi- Pigment production and growth on tryptic soy agar at 35°C tory for Canadian CF clinics was established in Vancouver. and 42°C were observed at 24 and 48 hours. Since that time, B. cepacia complex isolates from an estimated 75% of infected Canadian CF patients have been evaluated for Molecular Methods genomovar and species identity, random amplified polymor- phic DNA (RAPD) strain type, and putative markers of trans- Genomovar-Specific PCR for the recA Gene missibility. These data have permitted inferences about the Polymerase chain reaction (PCR) with selected recA prim- potential transmissibility of different strains and facilitated the ers was performed essentially as described (15,17). Tests were development of rational infection control guidelines. We done with the six recA subgroup genomovar-specific primers report data and conclusions from our observations to date. (15,17) and a seventh primer pair for genomovar VII as described (15,18). After amplification, 8 µL of each reaction Materials and Methods mixture was subjected to electrophoresis in 1.5% agarose gel. PCR products were photographed after ethidium bromide Patients and Clinics staining. B. cepacia complex strains that did not react with the Canadian CF clinics are linked through the Canadian Cys- specific primers described above were subjected to nucleotide tic Fibrosis Foundation, which collates annual summary data sequence analysis of the recA gene (17). Placement in the in its patient data registry. Approximately 3,200 patients with complex was then done phylogenetically by analysis of 500 bp CF receive care at 36 clinics in the 10 provinces. Each clinic of the N-terminal encoding sequence according to the algo- provides care for 20 to 300 patients (median age 17 years). rithm described (17). The number of patients with CF in Canada has increased by approximately 90 each year since 1994, although the median Speciation with the 16S rRNA Gene survival age has plateaued at approximately 30 years. Restriction fragment length polymorphism (RFLP) analy- In 1994, the Canadian B. cepacia Complex Research and sis of the 16S rRNA gene PCR product with the enzyme Dde1 Referral Repository was established at the British Columbia was performed as described (15,17). Research Institute for Children’s and Women’s Health in Van- couver. Each clinic director was notified about the new labora- Genotypic Identification of B. gladioli tory and encouraged to send archived and new isolates of B. A PCR reaction with primer pair LP1/LP4, directed toward cepacia complex to the Vancouver laboratory for strain typing a species-specific region of the 23S rRNA gene, was used (19). and confirmation of species identity (7). At least one isolate from each infected patient was solicited, as well as subsequent Strain Typing of B. cepacia Complex Isolates isolates that were considered phenotypically different. Each isolate was evaluated
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