Environmental Burkholderia cepacia complex isolates in human infections.Members of the Burkholderia cepacia complex Burkholderia cepacia complex (BCC), or simply Burkholderia cepacia is a group of catalase-producing, non-lactose-fermenting Gram-negative bacteria composed of at least nine different species, including B. cepacia, B. multivorans, B. (Bcc), found in many environments, are associated with clinical infections. Examining diverse species and strains from different environments with multilocus sequence typing Multilocus sequence typing (MLST) is a technique in molecular biology for the typing of multiple loci. The procedure characterizes isolates of bacterial species using the DNA sequences of internal fragments of multiple (usually seven) housekeeping genes. , we identified >20% of 381 clinical isolates as indistinguishable from those in the environment. This finding links the natural environment with the emergence of many Bcc infections. ********** The Burkholderia cepacia complex (Bcc) is a group of closely related gram-negative bacteria comprising at least 9 species (1). They are routinely isolated from the natural environment, where they can have a range of beneficial properties (2). However, these bacteria can also frequently cause fatal infections in vulnerable humans, such as those who have cystic fibrosis cystic fibrosis (sĭs`tĭk fībrō`sĭs), inherited disorder of the exocrine glands (see gland), affecting children and young people; median survival is 25 years in females and 30 years in males. (CF). Because Bcc bacteria are not normally carried as commensal commensal /com·men·sal/ (kom-men´sil) 1. living on or within another organism, and deriving benefit without harming or benefiting the host. 2. a parasite that causes no harm to the host. organisms, the main sources of infection are considered to be patient-to-patient spread (3,4); hospital settings, including medical devices and contaminated contaminated, v 1. made radioactive by the addition of small quantities of radioactive material. 2. made contaminated by adding infective or radiographic materials. 3. an infective surface or object. disinfectants; and the environment (5,6). Therefore, although Bcc species may have an important environmental role in agriculture and biotechnology industries, their use also represents a potential clinical risk to susceptible members of the community (7,8). All species of Bcc can be isolated from the environment in differing degrees (2). Similarly, all current Bcc species have been cultured from CF patient sputum sputum /spu·tum/ (spu´tum) [L.] expectoration; matter ejected from the trachea, bronchi, and lungs through the mouth. sputum cruen´tum bloody sputum. (2). Infection control measures have been implemented to reduce patient-to-patient transmission; although effective, these measures have not prevented the emergence of new infection. Thus, the environment could be acting as a constant nonpatient reservoir for infectious Bcc pathogens. Previous studies have reported the possibility of humans acquiring Bcc directly from natural environments (9,10). The most recent of these studies reported evidence that a B. cenocepacia strain, isolated from soil, was indistinguishable by several typing methods (pulsed-field gel electrophoresis gel electrophoresis n. Electrophoresis performed in a gel composed of agarose, polyacrylamide, or starch. [PFGE PFGE Pulsed-Field Gel Electrophoresis ] genomic fingerprinting and repetitive extragenic palindromic pal·in·dro·mic adj. Relapsing; recurring. [rep]-PCR) from isolates of the problematic CF lineage PHDC (10). The Study To evaluate how widespread the emergence of environmental isolates as causes of clinical infections may be, we used a highly discriminatory and transportable typing method to study isolates from several large bacterial culture collections. Multilocus sequence typing (MLST MLST Multi Locus Sequence Typing MLST Medical Logistics Support Team MLST Mini Losi Super Truck (1/18th scale radio control vehicle) ) is a relatively new technique based upon unambiguous sequence analysis of several housekeeping genes. Unlike previous methods for Bcc strain typing (10), MLST is not based on banding patterns but instead relies on the robust comparison of DNA sequence DNA sequence Genetics The precise order of bases–A,T,G,C–in a segment of DNA, gene, chromosome, or an entire genome. See Base pair, Base sequence analysis, Chromosome, Gene, Genome. information. This process facilitates both the identification and matching of identical clones as well as their evolutionary comparison to closely related strains. Using a recently validated MLST scheme (11), we analyzed a collection of 381 clinical isolates of all 9 currently reported Bee species, from 28 countries. A total of 187 distinct sequence types (STs) were identified from clinical isolates within this collection and compared with 233 environmental Bee isolates (113 STs). We found that 81 clinical isolates (encompassingl5 STs) were identical by MLST to a wide range of environmental isolates. This figure represents 21.5% of the clinical isolates examined (for clarity, a subset are shown in the Table; [12]). The resolution of strain identification offered by MLST is such that different isolates sharing the same ST (genotypically indistinguishable at all 7 loci loci [L.] plural of locus. loci Plural of locus, see there ) are defined as clones of the same strain (e.g., for a group of isolates within this collection, we have further validated this identity by cloning and sequencing up to 10 random fragments of DNA DNA: see nucleic acid. DNA or deoxyribonucleic acid One of two types of nucleic acid (the other is RNA); a complex organic compound found in all living cells and many viruses. It is the chemical substance of genes. ). The 15 STs identified from environmental and clinical sources belonged to 6 different Bcc species (Table): B. cepacia (4 STs), B. multivorans (2 STs), B. cenocepacia (3 STs), B. stabilis (2 STs), B. vietnamiensis (2 STs), and B. ambifaria (2 STs). Three B. cenocepacia STs also belonged to 2 different recA lineages defined within this species: IIIA IIIA Internet Information Infrastructure Architecture IIIA Integrated Intelligence Information Application IIIA International Imaging Industry Association (1 ST) and IIIB (2 STs). Conclusions STs occurring in both clinical and environmental niches were found in 6 of the 9 formally described Bcc; the greatest degree of overlap occurred in B. cepacia and B. stabilis (Figure). The proportion of STs not shared between clinical and environmental isolates varied for each Bcc species we examined. This finding may reflect the few clinical or environmental isolates for that species or high genetic diversity; a larger sample size is needed to find identical matches. Species dominated by clinical STs (>83% of STs) were B. multivorans, B. cenocepacia recA lineage IIIA, and B. dolosa. Those species containing mainly environmental STs (>80%) were B. ambifaria, B. anthina, and B. pyrrocinia (Figure). Although this distribution agrees with findings of previous studies (2), it also reflects the distribution of isolates within the collections from which isolates were obtained. [FIGURE OMITTED] Several ST matches between clinical and environmental isolates were of particular interest. MLST ST-10 was shared by B. cepacia J1050, a human isolate cultured in the United States United States, officially United States of America, republic (2005 est. pop. 295,734,000), 3,539,227 sq mi (9,166,598 sq km), North America. The United States is the world's third largest country in population and the fourth largest country in area. (Cleveland, Ohio "Cleveland" redirects here. For the Cleveland metropolitan area, see . For other uses, see Cleveland (disambiguation). Cleveland is a city in the U.S. state of Ohio and the county seat of Cuyahoga County, the most populous county in the state. ) and the type strain for B. cepacia ATCC ATCC American Type Culture Collection, see there 25416, isolated from an onion. This evidence of clonality augments the clonal relationship reported earlier (9) between ATCC 25416 and a UK isolate from a CF patient. The B. multivorans IST455 isolated from a CF patient's sputum in Portugal, as reported in a previous study (13) had the same sequence type (ST-375) as R-20526, which was isolated from the River Schelde in Belgium. B. cenocepacia recA lineage IIIA isolates with ST-32 (Table) were from 4 independent sources: POPR POPR Prototype Organic Power Reactor 8 (isolated from a radish radish, herbaceous plant (Raphanus sativus) belonging to the family Cruciferae (mustard family), with an edible, pungent root sliced in salads or used as a relish. in Mexico), BCC1118 (isolated from a UK non-CF patient infection), R-16597 (isolated from a CF patient in Belgium), and 5457 (isolated from a CF patient in the Czech Republic Czech Republic, Czech Česká Republika (2005 est. pop. 10,241,000), republic, 29,677 sq mi (78,864 sq km), central Europe. It is bordered by Slovakia on the east, Austria on the south, Germany on the west, and Poland on the north. ). ST-32 appears to be a globally distributed, predominantly clinical strain (A. Baldwin, unpub, data). The B. cenocepacia recA lineage IIIB isolates identified as ST-122 (Table) include the PHDC strains, predominant in US CF patients (AU 1054) and previously found in US soil (HI-2424) (10), and CEP CEP congenital erythropoietic porphyria. CEP abbr. congenital erythropoietic porphyria 0497, which was obtained from a leg wound in a non-CF patient in Canada. Together with a recent report of PHDC strains identified in Europe (14), the Canadian isolate in our study adds further weight to the identification of this ST as a globally distributed strain. MLST analysis of B. stabilis corroborated cor·rob·o·rate tr.v. cor·rob·o·rat·ed, cor·rob·o·rat·ing, cor·rob·o·rates To strengthen or support with other evidence; make more certain. See Synonyms at confirm. the high degree of clonality observed by PFGE fingerprint analysis in the original description of this species (15). However, MLST was further able to distinguish 8 STs among the 26 isolates examined, which indicates that MLST may be a more effective method than PFGE for epidemiologic analysis of B. stabilis. This increased resolution adds to the observation that 2 B. stabilis STs are globally distributed and isolated from clinical samples and an array of different niches, including domestic products, medical solutions, industrial process contaminants, and hospital devices. In summary, >20% of the clinical isolates we examined were indistinguishable by MLST from isolates from environmental sources. This finding suggests that conservation of intrinsic determinants necessary to thrive in environmental niches may confer an ability to colonize col·o·nize v. col·o·nized, col·o·niz·ing, col·o·niz·es v.tr. 1. To form or establish a colony or colonies in. 2. To migrate to and settle in; occupy as a colony. 3. susceptible humans. Further work is urgently required to more extensively investigate the emergence of pathogenic members of the Bcc in the natural environment and the risk for infection this may represent. Acknowledgments We thank Angela Marchbank and Lynne Richardson for technical support. This publication made use of the Bcc multilocus sequence typing website (http://pubmlst.org/bcc/) developed by Keith Jolley and hosted at the University of Oxford. This work was funded by Wellcome Trust The Wellcome Trust is a United Kingdom-based charity established in 1936 to administer the fortune of the American-born pharmaceutical magnate Sir Henry Wellcome. Its income was derived from what was originally called Burroughs Wellcome & Co, later renamed in the UK as the grant number 072853. The Trust also funded development of the website. References Coenye T, Vandamme P, Govan JR, LiPuma JJ. Taxonomy and identification of the Burkholderia cepacia complex. J Clin Microbiol. 2001;39:3427-36. (2.) Mahenthiralingam E, Urban TA, Goldberg JB. The multifarious multifarious adj., adv. reference to a lawsuit in which either party or various causes of action (claims based on different legal theories) are improperly joined together in the same suit. This is more commonly called "misjoinder." (See: misjoinder) , multireplicon Burkholderia cepacia complex. Nat Rev Microbiol. 2005;3:144-56. (3.) Govan JR, Brown PH, Maddison J, Doherty C J, Nelson JW, Dodd M, et al. Evidence for transmission of Pseudomonas Pseudomonas A genus of gram-negative, nonsporeforming, rod-shaped bacteria. Motile species possess polar flagella. They are strictly aerobic, but some members do respire anaerobically in the presence of nitrate. cepacia by social contact in cystic fibrosis. Lancet. 1993;342:15-9. (4.) LiPuma JJ, Dasen SE, Nielson DW, Stern RC, Stull TL. Person-to-person transmission of Pseudomonas cepacia between patients with cystic fibrosis. Lancet. 1990;336:1094-6. (5.) Hutchinson GR, Parker S, Pryor JA, Duncan-Skingle F, Hoffman PN, Hodson ME, et al. Home-use nebulizers: a potential primary source of Burkholderia cepacia Burkholderia cepacia Pseudomonas cepacia Bacteriology A bacterium found in the environment–eg, plants, water, soil, and in hospital environment, which may colonize the respiratory tract of Pts with cystic fibrosis; transmitted by direct physical and other colistin-resistant, gram-negative bacteria in patients with cystic fibrosis. J Clin Microbiol. 1996;34:584-7. (6.) Oie S, Kamiya A. Microbial microbial pertaining to or emanating from a microbe. microbial digestion the breakdown of organic material, especially feedstuffs, by microbial organisms. contamination of antiseptics and disinfectants. Am J Infect Control. 1996;24:389-95. (7.) Holmes A, Govan J, Goldstein R. Agricultural use of Burkholderia (Pseudomonas) cepacia: a threat to human health? Emerg Infect Dis. 1998;4:221-7. (8.) LiPuma JJ, Mahenthiralingam E. Commercial use of Burkholderia cepacia. Emerg Infect Dis. 1999;5:305-6. (9.) Govan JRW, Balendreau J, Vandamme P. Burkholderia cepacia Friend and foe Friend and Foe is the third release from the Portland, Oregon-based band Menomena. It was released January 23, 2007 by Barsuk Records. The cover art is designed by Craig Thompson, writer and illustrator of the award-winning graphic novel Blankets. . ASM (1) (Association for Systems Management) An international membership organization based in Cleveland, Ohio. Founded in 1947 and disbanded in 1996, it sponsored conferences in all phases of administrative systems and management. News. 2000;66:124-5. (10.) LiPuma JJ, Spilker T, Coenye T, Gonzalez CF. An epidemic Burkholderia cepacia complex strain identified in soil. Lancet. 2002;359:2002-3. (11.) Baldwin A, Mahenthiralingam E, Thickett KM, Honeybourne D, Maiden MC, Govan JR, et al. Multilocus sequence typing scheme that provides both species and strain differentiation for the Burkholderia cepacia complex. J Clin Microbiol. 2005;43: 4665-73. (12.) Coenye T, Vandamme P, LiPuma JJ, Govan JR, Mahenthiralingam E. 2003. Updated version of the Burkholderia cepacia complex experimental strain panel. J Clin Microbiol. 2003;41:2797-8. (13.) Cunha MV, Leitao JH, Mahenthiralingam E, Vandamme P, Lito L, Barreto C, et al. Molecular analysis of Burkholderia cepacia complex isolates from a Portuguese cystic fibrosis center: a 7-year study. J Clin Microbiol. 2003;41:4113-20. (14.) Coenye T, Spilker T, van Schoor A, LiPuma JJ, Vandamme P. Recovery of Burkholderia cenocepacia Burkholderia cenocepacia is a Gram-negative bacteria that is common in the environment and may cause disease in plants. It is an opportunistic pathogen and human infections are common in patients with cystic fibrosis and chronic granulomatous disease, and are often fatal. strain PHDC from cystic fibrosis patients in Europe. Thorax thorax, body division found in certain animals. In humans and other mammals it lies between the neck and abdomen and is also called the chest. The skeletal frame of the thorax is formed by the sternum (breastbone) and ribs in front and the dorsal vertebrae in back. . 2004;59:952-4. (15.) Vandamme P, Mahenthiralingam E, Holmes B, Coenye T, Hoste B, de Vos De Vos. For persons thus named, use Vos. P, et al. Identification and population structure of Burkholderia stabilis Burkholderia stabilis is a species of proteobacteria. sp. nov. (formerly Burkholderia cepacia genomovar IV). J Clin Microbiol. 2000;38:1042-7. Address for correspondence: Chris G. Dowson, Department of Biological Sciences, University of Warwick In the 1960s and 1970s, Warwick had a reputation as a politically radical institution.[3] More recently, the University has been seen as a favoured institution of the British New Labour government. , Coventry, CV4 7AL, Wales Wales, Welsh Cymru, western peninsula and political division (principality) of Great Britain (1991 pop. 2,798,200), 8,016 sq mi (20,761 sq km), west of England; politically united with England since 1536. The capital is Cardiff. , United Kingdom; email: c.g.dowson@warwick.ac.uk Adam Baldwin, * Eshwar Mahenthiralingam, ([dagger]) Pavel Drevinek, ([dagger] Peter Vandamme, ([double dagger double dagger n. A reference mark (  ) used in printing and writing. Also called diesis.Noun 1. ]) John R. Govan, ([section]) David J. Waine, * John J. LiPuma, ([paragraph]) Luigi Chiarini, # Claudia Dalmastri, # Deborah A. Henry, ** David P. Speert, ** David Honeybourne, ([dagger][dagger]) Martin C. J. Maiden, ([double dagger][double dagger]) and Chris G. Dowson * * Warwick University, Coventry, Wales, United Kingdom; ([dagger]) Cardiff University, Cardiff, England, United Kingdom; ([double dagger]) Universiteit Gent, Ghent, Belgium; ([section]) University of Edinburgh Medical School The University of Edinburgh Medical School is part of the College of Medicine and Veterinary Medicine of the University of Edinburgh. Teaching is mainly at The Royal Infirmary of Edinburgh in Little France, Edinburgh, Scotland. , Edinburgh, Scotland, United Kingdom; ([paragraph]) University of Michigan (body, education) University of Michigan - A large cosmopolitan university in the Midwest USA. Over 50000 students are enrolled at the University of Michigan's three campuses. The students come from 50 states and over 100 foreign countries. Medical School, Ann Arbor, Michigan  “Ann Arbor” redirects here. For other uses, see Ann Arbor (disambiguation). Ann Arbor is a city in the U.S. state of Michigan and the county seat of Washtenaw County. , USA; # Ente per le Nuove Tecnologie l'Energia e l'Ambiente Casaccia, Rome, Italy; ** University of British Columbia Locations Vancouver The Vancouver campus is located at Point Grey, a twenty-minute drive from downtown Vancouver. It is near several beaches and has views of the North Shore mountains. The 7. , Vancouver, British Columbia, Canada; ([dagger][dagger]) Birmingham Heartlands Hospital, Birmingham, England, United Kingdom; and ([double dagger][double dagger]) University of Oxford, Oxford, England, United Kingdom Dr Baldwin is a postdoctoral research fellow at the University of Warwick on a 3-year project funded by the Wellcome Trust. His main research interests are horizontal gene transfer “HGT” redirects here. For other uses, see HGT (disambiguation). Horizontal gene transfer (HGT), also Lateral gene transfer (LGT), is any process in which an organism transfers genetic material to another cell that is not its offspring. , pathogenicity islands, evolutionary biology, and epidemiology of bacterial populations.
Table. MLST analysis of the Burkholderia cepacia strains showing
their species, source, and geographic location *
Bcc species ST Isolate name Source
B. cepacia
1 ATCC 17759 ([dagger]) ENV
1 LMG 14087 NON
10 ATCC [25416.sup.T] ENV
10 J1050 NON
266 BC20 ENV
266 AU6671 NON
365 HI-3602 ENV
365 C8509 CF
365 AU3206 CF
B. multivorans
21 ATCC 17616 ([dagger]) ENV
21 AU0453 CF
21 C9140 CF
375 R-20526 ENV
375 IST455 CF
B. cenocepacia
IIIA
32 POPR8 ENV
32 5-457 CF
32 R-16597 CF
32 BCC1118 NON
B. cenocepacia
IIIB
37 BC-1 ENV
37 AU2362 CF
122 HI-2424 ENV
122 AU1054 CF
122 CEP0497 NON
B. stabilis
50 LMG 14294 ([dagger]) CF
50 R-16919 ENV
50 LMG 14086 ([dagger]) ENVH
51 HI-2482 ENV
51 ATCC 35254 ENVH
51 CEP0928 ENVH
51 LMG 14291 CF
51 LMG 7000 NON
B. vietnamiensis
61 J1702 ENVH
61 B000190 CF
61 J1712 NON
61 J1738 NON
61 J1742 NON
67 R-20590 ENV
67 D0774 CF
B. ambifaria
81 MVP-C2-4 ENV
81 B000250 ([dagger]) CF
77 [AMMD.sup.T] ENV
77 AU0212 CF
Year of
Bcc species Country Source of isolate isolation
B. cepacia
Trinidad Soil 1958
UK Wound 1988
USA Onion 1948
USA Human Before 1983
USA Water --
USA Wound --
USA Soil --
Canada Sputum 1999
USA Sputum --
B. multivorans
USA Soil Before 1966
USA Sputum --
Canada Sputum 2000
Belgium River water 2002
Portugal Sputum 2000
B. cenocepacia
IIIA
Mexico Radish --
Czech Republic Sputum 2002
Belgium Sputum 2001
UK Wound Before 1994
B. cenocepacia
IIIB
USA Maize rhizosphere --
USA Sputum 2000
USA Soil --
USA CF --
Canada Leg ulcer 1995
B. stabilis
Belgium Sputum 1993
Belgium Industrial --
UK Respirator 1970
USA Shampoo --
USA Medical solution 1980
USA Albuterol solution --
Belgium Sputum 1993
Sweden Blood 1983
B. vietnamiensis
USA Hospital equipment --
USA Sputum --
USA Wound --
USA Wound --
USA Wound --
Belgium River water 2002
Canada Sputum 2003
B. ambifaria
Italy Maize rhizosphere 1996
Australia Sputum 1994
USA Soil 1985
USA Sputum --
* MLST, multilocus sequence typing; Bcc, B. cepacia complex;
ST, sequence type; ENV, isolated from the environment; NON,
isolated from a non-cystic fibrosis (CF) patient; CF, isolated
from a CF patient; IIIA or IIIB, isolates belonging to B.
cenocepacia recA subgroup A or B, respectively; ENVH, isolated
from a hospital environment.
([dagger]) Panel strain (12); superscript T, type strain for
species.
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