Burkholderia and Emerging Pathogens in Cystic Fibrosis

John J. LiPuma

doi:10.1055/s-2004-815664

Seminars in Respiratory and Critical Care Medicine, Table of Contents

Semin Respir Crit Care Med 2003; 24(6): 681-692
DOI: 10.1055/s-2004-815664

Burkholderia and Emerging Pathogens in Cystic Fibrosis

John J. LiPuma

Department of Pediatrics and Communicable Diseases, University of Michigan Medical School, Ann Arbor, Michigan

Abstract

ABSTRACT

Persons with cystic fibrosis (CF) are susceptible to respiratory tract infection with a variety of bacterial species. Among these are several species in the genus Burkholderia (including members of the B. cepacia complex, B. gladioli, and B. pseudomallei), Stenotrophomonas maltophilia, Achromobacter (Alcaligenes) xylosoxidans, certain Ralstonia species, and species within the new genus Pandoraea. Enterobacteriaceae and several other rather unusual or novel species also can be found. Many of these species are closely related phylogenetically and have similar phenotypes, presenting a challenge to accurate laboratory identification. Although their role in contributing to pulmonary disease in CF is not clear, the incidence of infection by some of these species appears to be increasing. The broad-spectrum antimicrobial resistance typically exhibited by these species severely limits treatment options. Newly developed genotypic methods of identification will enable studies to better assess the epidemiology and natural history of these emerging pathogens in CF.

KEYWORDS

Burkholderia cepacia - Stenotrophomonas maltophilia - Achromobacter (Alcaligenes) xylosoxidans - Ralstonia spp. - Pandoraea spp.

Full Text

References

REFERENCES

1 Burkholder W H. Sour skin, a bacterial rot of onion bulbs. Phytopathol . 1950; 40 115-118
2 Yabuuchi E, Kosako Y, Oyaizu H. et al . 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 . 1992; 36 1251-1275
3 Coenye T, Vandamme P, Govan J RW, LiPuma J J. Taxonomy and identification of the Burkholderia cepacia complex. J Clin Microbiol . 2001; 39 3427-3436
4 Vandamme P, Holmes B, Vancanneyt M. et al . Occurrence of multiple genomovars of Burkholderia cepacia in cystic fibrosis patients and proposal of Burkholderia multivorans sp. nov. Int J Syst Bacteriol . 1997; 47 1188-1200
5 Vandamme P, Henry D, Coenye T. et al . Burkholderia anthina sp. nov. and Burkholderia pyrrocinia, two additional Burkholderia cepacia complex bacteria, may confound results of new molecular diagnostic tools. FEMS Immunol Med Microbiol . 2002; 33 143-149
6 LiPuma J J, Spilker T, Gill L H. et al . Disproportionate distribution of Burkholderia cepacia complex species and transmissibility markers in cystic fibrosis. Am J Respir Crit Care Med . 2001; 164 92-96
7 Agodi A, Mahenthiralingam E, Barchitta M. et al . Burkholderia cepacia complex infection in Italian patients with cystic fibrosis: prevalence, epidemiology and genomovar status. J Clin Microbiol . 2001; 39 2891-2896
8 Speert D P, Henry D, Vandamme P. et al . Epidemiology of Burkholderia cepacia complex in patients with cystic fibrosis, Canada. Emerg Infect Dis . 2002; 8 181-187
9 McMenamin J D, Zaccone T M, Coenye T. et al . Misidentification of Burkholderia cepacia in US cystic fibrosis treatment centers: an analysis of 1,051 recent sputum isolates. Chest . 2000; 117 1661-1665
10 Shreve M R, Butler S, Kaplowitz H J. et al . Impact of microbiology practice on cumulative prevalence of respiratory tract bacteria in patients with cystic fibrosis. J Clin Microbiol . 1999; 37 753-757
11 Kiska D L, Kerr A, Jones M C. et al . Accuracy of four commercial systems for identification of Burkholderia cepacia and other gram-negative nonfermenting bacilli recovered from patients with cystic fibrosis. J Clin Microbiol . 1996; 34 886-891
12 van Pelt C, Verduin C M, Goessens W H. et al . Identification of Burkholderia spp. in the clinical microbiology laboratory: comparison of conventional and molecular methods. J Clin Microbiol . 1999; 37 2158-2164
13 Shelly D B, Spilker T, Gracely E J. et al . Utility of commercial systems for identification of Burkholderia cepacia complex from cystic fibrosis sputum culture. J Clin Microbiol . 2000; 38 3112-3115
14 Brisse S, Stefani S, Verhoef J. et al . Comparative evaluation of the BD Phoenix and VITEK 2 automated instruments for identification of isolates of the Burkholderia cepacia complex. J Clin Microbiol . 2002; 40 1743-1748
15 LiPuma J J, Dulaney B J, McMenamin J D. et al . Development of rRNA-based PCR assays for identification of Burkholderia cepacia complex isolates recovered from cystic fibrosis patients. J Clin Microbiol . 1999; 37 3167-3170
16 Mahenthiralingam E, Bischof J, Byrne S K. et al . DNA-based diagnostic approaches for identification of Burkholderia cepacia complex, Burkholderia vietnamiensis, Burkholderia multivorans, Burkholderia stabilis, and Burkholderia cepacia genomovars I and III. J Clin Microbiol . 2000; 38 3165-3173
17 Henry D A, Mahenthiralingam E, Vandamme P. et al . Phenotypic methods for determining genomovar status of the Burkholderia cepacia complex. J Clin Microbiol . 2001; 39 1073-1078
18 Coenye T, LiPuma J J. Molecular epidemiology of Burkholderia species. Front Biosci . 2003; 8 E55-E67
19 LiPuma J J. Burkholderia cepacia: management issues and new insights. Clin Chest Med . 1998; 19 473-486
20 Johnson W M, Tyler S D, Rozee K R. Linkage analysis of geographic and clinical clusters in Pseudomonas cepacia infections by multilocus enzyme electrophoresis and ribotyping. J Clin Microbiol . 1994; 32 924-930
21 Pitt T L, Kaufmann M E, Patel P S. et al . Type characterization 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 . 1996; 44 203-210
22 Chen J S, Witzmann K A, Spilker T. et al . Endemicity and inter-city spread of Burkholderia cepacia genomovar III in cystic fibrosis. J Pediatr . 2001; 139 643-649
23 Liu L, Spilker T, Coenye T, LiPuma J J. Identification by subtractive hybridization of a novel insertion element specific for two wide spread epidemic Burkholderia cepacia genomovar III strains. J Clin Microbiol . 2003; 41 2471-2476
24 Sajjan U S, Sun L, Goldstein R, Forstner J F. 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 . 1995; 177 1030-1038
25 Mahenthiralingam E, Simpson D A, Speert D P. Identification and characterization of a novel DNA marker associated with epidemic Burkholderia cepacia strains recovered from patients with cystic fibrosis. J Clin Microbiol . 1997; 35 808-816
25a Biddick R, Spilker T , Martin A , LiPuma J J. Evidence of transmission of Burkholderia cepacia, B. multivorans, and B. dolosa among persons with cystic fibrosis. FEMS Microbiol Lett . 2003; 228 57-62
26 LiPuma J J. Burkholderia cepacia epidemiology and pathogenesis: implications for infection control. Curr Opin Pulm Med . 1998; 4 337-341
27 Ledson M J, Gallagher M J, Corkill J E. et al . Cross infection between cystic fibrosis patients colonized with Burkholderia cepacia Thorax . 1998; 53 432-436
28 Mahenthiralingam E, Vandamme P, Campbell M E. et al . Infection with Burkholderia cepacia complex genomovars in patients with cystic fibrosis: virulent transmissible strains of genomovar III can replace Burkholderia multivorans Clin Infect Dis . 2001; 33 1469-1475
28a Bernhardt S, Spilker T, Coffey T, LiPuma J J. Burkholderia cepacia complex in cystic fibrosis: frequency of strain replacement during chronic infection. Clin Infect Dis . 2003; 37 780-785
29 Saiman L, Siegel J. et al . Infection control recommendations for patients with cystic fibrosis: microbiology, important pathogens, and infection control practices to prevent patient-to-patient transmission. Infect Control Hosp Epidemiol . 2003; 24(suppl) S1-S53
30 Hutchison M L, Govan J R. Pathogenicity of microbes associated with cystic fibrosis. Microbes Infect . 1999; 1 1005-1014
31 Speert D P, Bond M, Woodman R C, Curnutte J T. Infection with Pseudomonas cepacia in chronic granulomatous disease: role of nonoxidative killing by neutrophils in host defense. J Infect Dis . 1994; 170 1524-1531
32 Saini L S, Galsworthy S B, John M A, Valvano M A. Intracellular survival of Burkholderia cepacia complex isolates in the presence of macrophage cell activation. Microbiol . 1999; 145 3465-3475
33 Chiu C-H, Ostry A, Speert D P. Invasion of murine respiratory epithelial cells in vivo by Burkholderia cepacia J Med Microbiol . 2001; 50 594-601
34 Huber B, Riedel K, Hentzer M. et al . The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiol . 2001; 147 2517-2528
35 Riedel K, Hentzer M, Geisenberger O. et al . N-acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiol . 2001; 147 3249-3262
36 Lewenza S, Conway B, Greenberg E P, Sokol P A. Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI. J Bacteriol . 1999; 181 748-756
37 Lewin L O, Byard P J, Davis P B. Effect of Pseudomonas cepacia colonization on survival and pulmonary function of cystic fibrosis patients. J Clin Epidemiol . 1990; 43 125-131
38 McCloskey M, McCaughan J, Redmond A OB, Elborn J S. Clinical outcome after acquisition of Burkholderia cepacia in patients with cystic fibrosis. Irish J Med Sci . 2001; 170 28-31
39 Whiteford M L, Wilkinson J D, McColl J H. et al . Outcome of Burkholderia (Pseudomonas) cepacia colonization in children with cystic fibrosis following a hospital outbreak. Thorax . 1995; 50 1194-1198
40 Corey M, Farewell V. Determinants of mortality from cystic fibrosis in Canada, 1970-1989. Am J Epidemiol . 1996; 143 1007-1017
41 Liou T G, Adler F R, FitzSimmons S C. et al . Predictive 5-year survivorship model of cystic fibrosis. Am J Epidemiol . 2001; 153 345-352
42 Isles A, Maclusky I, Corey M. et al . Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J Pediatr . 1984; 104 206-210
43 DeSoyza A, McDowell A, Archer L. et al . Burkholderia cepacia complex genomovars and pulmonary transplantation outcomes in patients with cystic fibrosis. Lancet . 2001; 358 1780-1781
44 Aris R M, Routh J, LiPuma J J. et al . Burkholderia cepacia complex in cystic fibrosis patients after lung transplantation: survival linked to genomovar type. Am J Respir Crit Care Med . 2001; 164 2102-2106
45 Cox A D, Wilkinson S G. Ionizing groups in lipopolysaccharides of Pseudomonas cepacia in relation to antibiotic resistance. Mol Microbiol . 1991; 5 641-646
46 Chiesa C, Labrozzi P H, Aronoff S C. Decreased baseline beta-lactamase production and inducibility associated with increased piperacillin susceptibility of Pseudomonas cepacia isolated from children with cystic fibrosis. Pediatr Res . 1986; 20 1174-1177
47 Burns J L, Lien D M, Hedin L A. Isolation and characterization of dihydrofolate reductase from trimethoprim-susceptible and trimethoprim-resistant Pseudomonas cepacia Antimicrob Agents Chemother . 1989; 33 1247-1251
48 Burns J L, Wadsworth C D, Barry J J, Goodall C P. Nucleotide sequence analysis of a gene from Burkholderia (Pseudomonas) cepacia encoding an outer membrane lipoprotein involved in multiple antibiotic resistance. Antimicrob Agents Chemother . 1996; 40 307-313
49 Aaron S D, Ferris W, Henry D A. et al . Multiple combination bactericidal antiobiotic testing for patients with cystic fibrosis infected with Burkholderia cepacia Am J Respir Crit Care Med . 2000; 161 1206-1212
50 Christenson J C, Welch D F, Mukwaya G. et al . Recovery of Pseudomonas gladioli from respiratory tract specimens of patients with cystic fibrosis. J Clin Microbiol . 1989; 27 270-273
51 Barker P M, Wood R E, Gilligan P H. Lung infection with Burkholderia gladioli in a child with cystic fibrosis: acute clinical and spirometric deterioration. Pediatr Pulmonol . 1997; 23 123-125
52 Jones A M, Dodd M E, Webb A K. Burkholderia cepacia: current clinical issues, environmental controversies and ethical dilemmas. Eur Respir J . 2001; 17 295-301
53 Khan S U, Gordon S M, Stillwell P C. et al . Empyema and bloodstream infection caused by Burkholderia gladioli in a patient with cystic fibrosis after lung transplantation. Pediatr Infect Dis J . 1996; 15 637-639
54 Kanj S S, Tapson V, Davis R D. et al . Infections in patients with cystic fibrosis following lung transplantation. Chest . 1997; 112 924-930
55 Wilsher M L, Kolbe J, Morris A J, Welch D F. Nosocomial acquisition of Burkholderia gladioli in patients with cystic fibrosis. Am J Respir Crit Care Med . 1997; 155 1436-1440
56 Clode F E, Metherell L A, Pitt T L. Nosocomial acquisition of Burkholderia gladioli in patients with cystic fibrosis. Am J Respir Crit Care Med . 1999; 160 374-375
57 Whitby P W, Pope L C, Carter K B. et al . Species specific PCR as a tool for the identification of Burkholderia gladioli J Clin Microbiol . 2000; 38 282-285
58 Chaowagul W, White N J, Dance D A. et al . Melioidosis: a major cause of community-acquired septicemia in northeastern Thailand. J Infect Dis . 1989; 159 890-899
59 Smith C J. Human melioidosis: an emerging medical problem. Mircen J . 1987; 3 343-366
60 Mays E E, Ricketts E A. Melioidosis: recrudescence associated with bronchogenic carcinoma twenty-six years following initial geographic exposure. Chest . 1975; 68 261-263
61 Dance D A. Melioidosis. Curr Opin Infect Dis . 2002; 15 127-132
62 Leelarasamee A, Bovornkitti S. Melioidosis: review and update. Rev Infect Dis . 1989; 11 413-425
63 Dance D A, Smith M D, Aucken H M, Pitt T L. Imported melioidosis in England and Wales. Lancet . 1999; 353 208
64 Schulin T, Steinmetz I. Chronic melioidosis in a patient with cystic fibrosis. J Clin Microbiol . 2001; 39 1676-1677
65 Visca P, Cazzola G, Petrucca A, Braggion C. Travel-associated Burkholderia pseudomallei infection (melioidosis) in a patient with cystic fibrosis: a case report. Clin Infect Dis . 2001; 32 E15-E16
66 Holland D J, Wesley A, Drinkovic D, Currie B J. Cystic fibrosis and Burkholderia pseudomallei infection: an emerging problem?. Clin Infect Dis . 2002; 35 e138-e140
67 Swings J, De Vos P, Van den Mooter M, De Ley J. Transfer of Pseudomonas maltophilia Hugh 1981 to the genus Xanthomonas as Xanthomonas maltophilia (Hugh 1981) comb. nov. Int J Syst Bacteriol . 1983; 33 409-413
68 Palleroni N J, Bradbury J F. Stenotrophomonas, a new bacterial genus for Xanthomonas maltophilia (Hugh 1980) Swings et al., 1983. Int J Syst Bacteriol . 1993; 43 606-609
69 Burdge D R, Noble M A, Campbell M E. et al . Xanthomonas maltophilia misidentified as Pseudomonas cepacia in cultures of sputum from patients with cystic fibrosis: a diagnostic pitfall with major clinical implications. Clin Infect Dis . 1995; 20 445-448
70 Whitby P W, Carter K B, Burns J L. et al . Identification and detection of Stenotrophomonas maltophilia by rRNA-directed PCR. J Clin Microbiol . 2000; 38 4305-4309
71 Khardori N, Elting L, Wong E. et al . Nosocomial infections due to Xanthomonas maltophilia (Pseudomonas maltophilia) in patients with cancer. Rev Infect Dis . 1990; 12 997-1003
72 Villarino M E, Stevens L E, Schable B. et al . Risk factors for epidemic Xanthomonas maltophilia infection/colonization in intensive care unit patients. Infect Control Hosp Epidemiol . 1992; 13 201-206
73 Muder R R, Harris A P, Muller S. et al . Bacteremia due to Stenotrophomonas (Xanthomonas) maltophilia: a prospective, multicenter study of 91 episodes. Clin Infect Dis . 1996; 22 508-512
74 Alfieri N, Ramotar K, Armstrong P. et al . Two consecutive outbreaks of Stenotrophomonas maltophilia (Xanthomonas maltophilia) in an intensive-care unit defined by restriction fragment-length polymorphism typing. Infect Control Hosp Epidemiol . 1999; 20 553-556
75 Hanes S D, Demirkan K, Tolley E. et al . Risk factors for late-onset nosocomial pneumonia caused by Stenotrophomonas maltophilia in critically ill trauma patients. Clin Infect Dis . 2002; 35 228-235
76 Spencer R C. The emergence of epidemic, multiple-antibiotic-resistant Stenotrophomonas (Xanthomonas) maltophilia and Burkholderia (Pseudomonas) cepacia J Hosp Infect . 1995; 30(suppl) 453-464
77 Denton M, Kerr K G. Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia Clin Microbiol Rev . 1998; 11 57-80
78 Sattler C A, Mason Jr O E, Kaplan S L. Nonrespiratory Stenotrophomonas maltophilia infection at a children's hospital. Clin Infect Dis . 2000; 31 1321-1330
79 Talmaciu I, Varlotta L, Mortensen J, Schidlow D V. Risk factors for emergence of Stenotrophomonas maltophilia in cystic fibrosis. Pediatr Pulmonol . 2000; 30 10-15
80 Demko C A, Stern R C, Doershuk C F. Stenotrophomonas maltophilia in cystic fibrosis: incidence and prevalence. Pediatr Pulmonol . 1998; 25 304-308
81 Burns J L, Emerson J, Stapp J R. et al . Microbiology of sputum from patients at cystic fibrosis centers in the United States. Clin Infect Dis . 1998; 27 158-163
82 Graff G R, Burns J L. Factors affecting the incidence of Stenotrophomonas maltophilia isolation in cystic fibrosis. Chest . 2002; 121 1754-1760
83 Ballestero S, Virseda I, Escobar H. et al . Stenotrophomonas maltophilia in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis . 1995; 14 728-729
84 Elting L S, Khardori N, Bodey G P, Fainstein V. Nosocomial infection caused by Xanthomonas maltophilia: a case-control study of predisposing factors. Infect Control Hosp Epidemiol . 1990; 11 134-138
85 Sanyal S C, Mokaddas E M. The increase in carbapenem use and emergence of Stenotrophomonas maltophilia as an important nosocomial pathogen. J Chemother . 1999; 11 28-33
86 Schaumann R, Stein K, Eckhardt C. et al . Infections caused by Stenotrophomonas maltophilia: a prospective study. Infection . 2001; 29 205-208
87 Carmeli Y, Samore M H. Comparison of treatment with imipenem versus ceftazidime as a predisposing factor for nosocomial acquisition of Stenotrophomonas maltophilia: a historical cohort study. Clin Infect Dis . 1997; 24 1131-1134
88 Denton M, Todd N J, Littlewood J M. Role of anti-pseudomonal antibiotics in the emergence of Stenotrophomonas maltophilia in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis . 1996; 15 402-405
89 Hauben L, Vauterin L, Moore E R. et al . Genomic diversity of the genus Stenotrophomonas Int J Syst Bacteriol . 1999; 49(pt 4) 1749-1760
90 Agger W A, Cogbill T H, Busch H. et al . Wounds caused by corn-harvesting machines: an unusual source of infection due to gram-negative bacilli. Rev Infect Dis . 1986; 8 927-931
91 Klausner J D, Zukerman C, Limaye A P, Corey L. Outbreak of Stenotrophomonas maltophilia bacteremia among patients undergoing bone marrow transplantation: association with faulty replacement of handwashing soap. Infect Control Hosp Epidemiol . 1999; 20 756-758
92 Weber D J, Rutala W A, Blanchet C N. et al . Faucet aerators: a source of patient colonization with Stenotrophomonas maltophilia Am J Infect Control . 1999; 27 59-63
93 Denton M, Todd N J, Kerr K G. et al . Molecular epidemiology of Stenotrophomonas maltophilia isolated from clinical specimens from patients with cystic fibrosis and associated environmental samples. J Clin Microbiol . 1998; 36 1953-1958
94 Krzewinski J W, Nguyen C D, Foster J M, Burns J L. Use of random amplified polymorphic DNA PCR to examine epidemiology of Stenotrophomonas maltophilia and Achromobacter (Alcaligenes) xylosoxidans from patients with cystic fibrosis. J Clin Microbiol . 2001; 39 3597-3602
95 Senol E, DesJardin J, Stark P C. et al . Attributable mortality of Stenotrophomonas maltophilia bacteremia. Clin Infect Dis . 2002; 34 1653-1656
96 Gladman G, Connor P J, Williams R F, David T J. Controlled study of Pseudomonas cepacia and Pseudomonas maltophilia in cystic fibrosis. Arch Dis Child . 1992; 67 192-195
97 Karpati F, Malmborg A S, Alfredsson H. et al . Bacterial colonisation with Xanthomonas maltophilia: a retrospective study in a cystic fibrosis patient population. Infection . 1994; 22 258-263
98 Goss C H, Otto K, Aitken M L, Rubenfeld G D. Detecting Stenotrophomonas maltophilia does not reduce survival of patients with cystic fibrosis. Am J Respir Crit Care Med . 2002; 166 356-361
99 Schmitz F J, Verhoef J, Fluit A C. Comparative activities of six different fluoroquinolones against 9,682 clinical bacterial isolates from 20 European university hospitals participating in the European SENTRY surveillance programme. The SENTRY participants group. Int J Antimicrob Agents . 1999; 12 311-317
100 Ratnalingham R A, Peckham D, Denton M. et al . Stenotrophomonas maltophilia bacteraemia in two patients with cystic fibrosis associated with totally implantable venous access devices. J Infect . 2002; 44 53-55
101 Krueger T S, Clark E A, Nix D E. In vitro susceptibility of Stenotrophomonas maltophilia to various antimicrobial combinations. Diagn Microbiol Infect Dis . 2001; 41 71-78
102 Klinger J D, Thomassen M J. Occurrence and antimicrobial susceptibility of gram-negative nonfermentative bacilli in cystic fibrosis patients. Diagn Microbiol Infect Dis . 1985; 3 149-158
103 Vandamme P, Heyndrickx M, Vancanneyt M. et al . Bordetella trematum sp. nov., isolated from wounds and ear infections in humans, and reassessment of Alcaligenes denitrificans Ruger and Tan 1983. Int J Syst Bacteriol . 1996; 46 849-858
104 Yabuuchi E, Kawamura Y, Kosako Y, Ezaki T. Emendation of genus Achromobacter and Achromobacter xylosoxidans (Yabuuchi and Yano) and proposal of Achromobacter ruhlandii (Packer and Vishniac) comb. nov., Achromobacter piechaudii (Kiredjian et al.) comb. nov., and Achromobacter xylosoxidans subsp. denitrificans (Ruger and Tan) comb. nov. Microbiol Immunol . 1998; 42 429-438
105 Duggan J M, Goldstein S J, Chenoweth C E. et al . Achromobacter xylosoxidans bacteremia: report of four cases and review of the literature. Clin Infect Dis . 1996; 23 569-576
106 Vu-Thien H, Darbord J C, Moissenet D. et al . Investigation of an outbreak of wound infections due to Alcaligenes xylosoxidans transmitted by chlorhexidine in a burns unit. Eur J Clin Microbiol Infect Dis . 1998; 17 724-726
107 Weitkamp J-H, Tang Y-W, Hass D W. et al . Recurrent Achromobacter xylosoxidans bacteremia associated with persistent lymph node infection in a patient with hyper-immunoglobulin M syndrome. Clin Infect Dis . 2000; 31 1183-1187
108 Liu L, Coenye T, Burns J L. et al . Ribosomal DNA-directed PCR for identification of Achromobacter (Alcaligenes) xylosoxidans recovered from sputum samples from cystic fibrosis patients. J Clin Microbiol . 2002; 40 1210-1213
109 Kay S E, Clark R A, White K L, Peel M M. Recurrent Achromobacter piechaudii bacteremia in a patient with hematological malignancy. J Clin Microbiol . 2001; 39 808-810
110 Tan K, Conway S P, Brownlee K G. et al . Alcaligenes infection in cystic fibrosis. Pediatr Pulmonol . 2002; 34 101-104
111 Saiman L, Chen Y, Tabibi S. et al . Identification and antimicrobial susceptibility of Alcaligenes xylosoxidans isolated from patients with cystic fibrosis. J Clin Microbiol . 2001; 39 3942-3945
112 Dunne Jr M W, Maisch S. Epidemiological investigation of infections due to Alcaligenes species in children and patients with cystic fibrosis: use of repetitive-element-sequence polymerase chain reaction. Clin Infect Dis . 1995; 20 836-841
113 Vu-Thien H, Moissenet D, Valcin M. et al . Molecular epidemiology of Burkholderia cepacia, Stenotrophomonas maltophilia, and Alcaligenes xylosoxidans in a cystic fibrosis center. Eur J Clin Microbiol Infect Dis . 1996; 15 876-879
114 Moissenet D, Baculard A, Valcin M. et al . Colonization by Alcaligenes xylosoxidans in children with cystic fibrosis: a retrospective clinical study conducted by means of molecular epidemiological investigation. Clin Infect Dis . 1997; 24 274-275
115 Peltroche-Llacsahuanga H, Haase G, Kentrup H. Persistent airway colonization with Alcaligenes xylosoxidans in two brothers with cystic fibrosis. Eur J Clin Microbiol Infect Dis . 1998; 17 132-134
116 Coenye T, Falsen E, Hoste B. et al . Description of Pandoraea gen. nov. with Pandoraea apista sp. nov., Pandoraea pulmonicola sp. nov., Pandoraea pnomenusa sp. nov., Pandoraea sputorum sp. nov. and Pandoraea norimbergensis comb. nov. Int J Syst Evol Microbiol . 2000; 50 887-899
117 Daneshvar M I, Hollis D G, Steigerwalt A G. et al . Assignment of CDC weak oxidizer group 2 (WO-2) to the genus Pandoraea and characterization of three new Pandoraea genomospecies. J Clin Microbiol . 2001; 39 1819-1826
118 Stryjewski M E, LiPuma J J, Messier R H, Reller L B, Alexander B D. Sepsis, multiple organ failure, and death due to Pandoraea pnomenusa infection after lung transplantation. J Clin Microbiol . 2003; 41 2255-2257
119 Coenye T, Liu L, Vandamme P, LiPuma J J. Identification of Pandoraea species by 16S ribosomal DNA-based PCR assays. J Clin Microbiol . 2001; 39 4452-4455
120 Coenye T, LiPuma J J. Use of the gyrB gene for identification of Pandoreae species. FEMS Microbiol Lett . 2002; 208 15-19
121 Yabuuchi E, Kosako Y, Yano I. et al . Transfer of two Burkholderia and an Alcaligenes species to Ralstonia gen. nov.: proposal of Ralstonia pickettii (Ralston, Palleroni and Doudoroff 1973) comb. nov., Ralstonia solanacearum (Smith 1896) comb. nov. and Ralstonia eutropha (Davis 1969) comb. nov. Microbiol Immunol . 1995; 39 897-904
122 Boutros N, Gonullu N, Casetta A. et al . Ralstonia pickettii traced in blood culture bottles. J Clin Microbiol . 2002; 40 2666-2667
123 Coenye T, Vandamme P, LiPuma J J. Infection by Ralstonia species in cystic fibrosis patients: identification of R pickettii and R. mannitolilytica by polymerase chain reaction. Emerg Infect Dis . 2002; 8 692-696
124 Vandamme P, Goris J, Coenye T. et al . Assignment of centers for disease control group IVc-2 to the genus Ralstonia as Ralstonia paucula sp. nov. Int J Syst Bacteriol . 1999; 49 663-669
125 Coenye T, Falsen E, Vancanneyt M. et al . Classification of Alcaligenes faecalis-like isolates from the environment and human clinical samples as Ralstonia gilardii sp. nov. Int J Syst Bacteriol . 1999; 49 405-413
126 Vaneechoutte M, De Baere T, Wauters G. et al . One case each of recurrent meningitis and hemoperitoneum infection with Ralstonia mannitolilytica J Clin Microbiol . 2001; 39 4588-4590
127 Wauters G, Claeys G, Verschraegen G. et al . Case of catheter sepsis with Ralstonia gilardii in a child with acute lymphoblastic leukemia. J Clin Microbiol . 2001; 39 4583-4584
128 De Baere T, Steyaert S, Wauters G. et al . Classification of Ralstonia pickettii biovar 3/'thomasii' strains (Pickett 1994) and of new isolates related to nosocomial recurrent meningitis as Ralstonia mannitolytica sp. nov. Int J Syst Evol Microbiol . 2001; 51 547-558
129 Coenye T, Goris J, De Vos P, Vandamme P, LiPuma J J. Classification of Ralstonia pickettii-like isolates from the environment and clinical samples as Ralstonia insidiosa sp. nov. Int J Syst Evol Microbiol . 2003; 53 1075-1080
130 Coenye T, Vandamme P, LiPuma J J. Ralstonia respiraculi sp. nov., isolated from the respiratory tract of cystic fibrosis patients. Int J Syst Evol Microbiol . 2003; 53 1339-1342
131 Coenye T, Goris J, Spilker T. et al . Characterization of unusual bacteria isolated from respiratory secretions of cystic fibrosis patients and description of Inquilinus limosus gen. nov., sp. nov. J Clin Microbiol . 2002; 40 2062-2069
132 Canton R, Morosini M I, Ballestero S. et al . Lung colonization with Enterobacteriaceae producing extended-spectrum beta-lactamases in cystic fibrosis patients. Pediatr Pulmonol . 1997; 24 213-217