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Journal of Clinical Microbiology, October 2001, p. 3597-3602, Vol. 39, No. 10
Division of Infectious Disease, Department of
Pediatrics, Children's Hospital and Regional Medical Center and
University of Washington, Seattle, Washington
Received 26 February 2001/Returned for modification 26 March
2001/Accepted 23 July 2001
Stenotrophomonas maltophilia and
Achromobacter (Alcaligenes)
xylosoxidans have been increasingly recognized as a
cause of respiratory tract colonization in cystic fibrosis (CF).
Although both organisms have been associated with progressive
deterioration of pulmonary function, demonstration of causality is
lacking. To examine the molecular epidemiology of S.
maltophilia and A. xylosoxidans in CF, isolates
from patients monitored for up to 2 years were fingerprinted using a
PCR-based randomly amplified polymorphic DNA (RAPD-PCR) method.
Sixty-one of 69 CF centers screened had 183 S.
maltophilia culture-positive patients, and 46 centers had 92 A. xylosoxidans-positive patients. At least one isolate
from each patient was genotyped, and patients with Stenotrophomonas
maltophilia and Achromobacter (Alcaligenes)
xylosoxidans are aerobic, nonfermentative, gram-negative
bacilli that are found in a wide variety of aquatic, soil, and
rhizosphere environments. Both organisms have been isolated from
hospital sources, and they have been increasingly recognized as
nosocomial pathogens, particularly for immunocompromised patients
(7, 13, 14, 19, 22, 31, 38, 41). Recent evidence suggests that they may also be emerging pathogens in cystic fibrosis (CF) patients (1, 4, 6, 9, 12, 28).
The prevalence of S. maltophilia in the respiratory tract of
patients with CF has increased in recent years, with some clinics reporting rates in excess of 30% (1, 9). Interestingly, the source of the majority of S. maltophilia strains
colonizing the respiratory tracts of CF patients cannot be linked to
previously identified nosocomial sources, suggesting multiple,
independent acquisitions from a variety of environmental sources
(10). The data on A. xylosoxidans in CF is less
complete, but the prevalence in CF patients may be as high as 8.7%
(4). There are no studies identifying the source of
A. xylosoxidans in CF patients, although nebulizers and
respiratory therapy equipment have been implicated in nosocomial
respiratory tract infections in non-CF patients (7).
Lung infection with gram-negative organisms is an important cause of
morbidity and mortality in CF. Two of the most important CF pathogens,
Pseudomonas aeruginosa and Burkholderia cepacia, are persistently isolated from CF sputum. However, very different epidemiological scenarios exist for B. cepacia and P. aeruginosa. Cross-infection with P. aeruginosa within a
CF center is only rarely seen (26, 37), whereas epidemic
spread of some strains of B. cepacia has been clearly
demonstrated (17, 24, 25, 39).
The epidemiology of S. maltophilia and A. xylosoxidans in patients with CF is not well understood. To date,
no genotyping study has analyzed isolates of these organisms from
multiple patients at different CF centers in order to determine whether
these isolates are closely related or unique. It is also unknown
whether patients are persistently colonized, with the organism escaping
detection on certain cultures, or whether a cycle of acquisition and
clearing is occurring. It is important to investigate these questions, because clinicians report individual patients who exhibit deterioration of pulmonary function associated with isolation of these organisms from
CF sputum. Establishing the role of S. maltophilia and
A. xylosoxidans in CF lung infections could have significant
treatment implications, because these organisms are often highly
resistant to various antibiotics, including To examine the epidemiology of S. maltophilia and A. xylosoxidans we used random amplified polymorphic DNA PCR
(RAPD-PCR). This technique utilizes a single, arbitrary oligonucleotide
primer selected for its ability to discriminate among epidemiologically distinct isolates. This random primer anneals to multiple sites in the
genome, resulting in a reproducible banding pattern. RAPD-PCR has
previously been shown to be discriminatory for typing bacterial isolates from the lungs of patients with CF, including P. aeruginosa and B. cepacia (25, 26).
Several authors have reported its utility in the typing of nosocomial
outbreaks of S. maltophilia (21). Both
enterobacterial repetitive intergenic consensus (ERIC) PCR and
repetitive extragenic palindromic PCR have been used to type a small
outbreak of A. xylosoxidans from the lungs of children with
and without CF (12). ERIC PCR and repetitive extragenic palindromic PCR have also been compared with pulsed-field gel electrophoresis for the typing of nosocomial outbreaks and CF isolates
of A. xylosoxidans (23, 28).
The isolates for this study were obtained from a collection of
bacterial isolates from patients enrolled in paired clinical trials of
inhaled tobramycin (6, 32). This collection of sequential
isolates from a large number of CF patients from many centers across
the United States offered the unique opportunity to investigate the
molecular epidemiology of these emerging pathogens. The overall
objectives of the study were (i) to determine whether specific clones
of S. maltophilia and A. xylosoxidans could be identified at difference CF centers across the United States, (ii) to
examine whether individual patients within a CF center shared common
genotypes, and (iii) to identify patterns of organism acquisition,
namely, do patients persistently have the same isolate or are different
ones acquired and lost over time?
Bacterial isolates and microbiological methods.
The clinical
trials of inhaled tobramycin (6, 32) enrolled 520 patients
at 69 CF centers in the United States. All gram-negative isolates from
sputum and oropharyngeal cultures obtained during these trials were
saved and identified using standard techniques, including the use of a
biochemical panel for the identification of non-P.
aeruginosa, non-lactose-fermenting gram-negative bacilli (36). Following identification, isolates were catalogued
and frozen at Isolation of genomic DNA
A single colony was
inoculated into 2 ml of L broth in a 20-ml glass tube and grown
overnight in a shaking incubator at 37°C. After harvest by
centrifugation, the bacterial pellet was resuspended in 50 mM
glucose-25 mM EDTA-10 mM Tris-Cl, pH 8.0. Genomic DNA was isolated by
a modified alkaline lysis preparation, which included an overnight
digestion with pronase to degrade extracellular nucleases. Other than
this modification, this was a standard preparation that used ammonium
acetate and chloroform, to remove proteins and polysaccharides, and
isopropanol, to precipitate genomic DNA (35). The
resulting DNA pellet was resuspended in H2O containing RNase and quantified by A260. All
preparations were frozen at RAPD typing
The RAPD primer sequences were
provided by Eshwar Mahenthiralingam, University of British Columbia,
Vancouver, Canada, and were as follows: for primer 270, 5'
TGCGCGCGGG 3'; for primer 272, 5' AGCGGGCCAA
3'. Both primers were used to produce discriminatory polymorphisms from CF isolates of P. aeruginosa and
B. cepacia, organisms with a G+C content similar to that
of S. maltophilia and A. xylosoxidans
(25, 26). Thus, they were screened for their utility with
12 S. maltophilia and 13 A. xylosoxidans
isolates each from a different CF center. This confirmed the ability of the primers to produce discriminatory polymorphisms with these organisms. Primer 270 was initially used to type the isolates in this
study; primer 272 was used for confirmation of identity in strains with
similar patterns using primer 270.
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.10.3597-3602.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Use of Random Amplified Polymorphic DNA PCR To
Examine Epidemiology of Stenotrophomonas maltophilia and
Achromobacter (Alcaligenes)
xylosoxidans from Patients with Cystic
Fibrosis
ABSTRACT
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
10 positive
cultures (12 S. maltophilia cultures, 15 A.
xylosoxidans cultures) had serial isolates genotyped. In
addition, centers with multiple culture-positive patients were examined
for evidence of shared clones. There were no instances of shared
genotypes among different CF centers. Some patients demonstrated
isolates with a single genotype throughout the observation period, and others had intervening or sequential genotypes. At the six centers with
multiple S. maltophilia culture-positive patients and
the seven centers with multiple A. xylosoxidans-positive
patients, there were three and five instances of shared genotypes,
respectively. The majority of shared isolates were from pairs who were
siblings or otherwise epidemiologically linked. These findings suggest RAPD-PCR typing can distinguish unique CF isolates of S.
maltophilia and A. xylosoxidans,
person-to-person transmission may occur, there are not a small number
of clones infecting CF airways, and patients with long-term
colonization may either have a persistent organism or may acquire
additional organisms over time.
INTRODUCTION
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
-lactams, quinolones,
aminoglycosides, and carbapenems (16, 18, 27, 33) that are
commonly used for the management of CF lung infections. The increase in
prevalence of S. maltophilia in the lungs of CF patients has
been associated with the extensive use of antipseudomonal antibiotics
for early treatment of P. aeruginosa colonization and for
suppression of chronic P. aeruginosa respiratory tract
infections (11). Parallel data are unavailable for
A. xylosoxidans. Molecular typing may contribute to our
knowledge of the epidemiology of these infections in CF, thus allowing
the development of strategies to prevent their acquisition.
MATERIALS AND METHODS
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Introduction
Materials and Methods
Results
Discussion
References
80°C in 0.5 ml of sterile skim milk. Isolates
identified as S. maltophilia or A. xylosoxidans
were recovered from frozen stocks and grown on Luria (L) agar with 24 to 48 h of incubation at 37°C for use in the present study.
80°C until use.
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RESULTS |
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S. maltophilia isolates. There were a total of 183 S. maltophilia culture-positive patients, with a range of 0 to 21 isolates per patient. Seventy-seven patients had a single isolation of the organism over a 2-year period. Of these 77, 15 were from throat swabs (19%) and 62 were from sputum cultures. Of the S. maltophilia-positive cultures overall, the percentage of isolates from throat swabs was similar (16%).
Sixty-one of the 69 CF centers in the study had patients with respiratory cultures positive for S. maltophilia. There were 16 centers with a single culture-positive patient and 10 sites with five or more culture-positive patients. From 55 centers, a single isolate from each patient was amplified. Isolates from the additional six sites, each with five or more culture-positive patients, were examined in greater detail with multiple isolates from each patient typed. A total of 309 isolates from 168 patients were examined.A. xylosoxidans isolates. The respiratory tract cultures from 92 patients grew A. xylosoxidans. Forty-five patients had a single isolation of the organism; five were from throat swabs (11%), compared with 9% of isolates from throat swabs in the A. xylosoxidans positive specimens, overall.
Forty-six of the study centers were found to have A. xylosoxidans culture-positive patients. There were 12 centers with only a single patient whose cultures grew A. xylosoxidans and three centers that had five or more culture-positive patients. From 33 of the 46 sites, a single isolate from each patient with A. xylosoxidans was amplified, resulting in discriminatory polymorphisms. The remaining 13 CF centers were investigated in more detail, either because they had a large number of patients with the organism or because a single patient had multiple isolates. A total of 290 isolates from 92 patients were examined.Reproducibility of RAPD analysis. Primers 270 and 272 gave reproducible polymorphisms suitable for strain differentiation, ranging from 1 to 14 bands over an approximate size range of 200 to 3,000 bp. To demonstrate genotype stability, three unique isolates of each organism from different centers were passaged consecutively on L agar five times, with RAPD-PCR performed after each passage. Both sets of organisms showed stable genotypes with both primers following each passage, as shown by identical polymorphisms.
Molecular epidemiology. To investigate the genetic relatedness among isolates from patients at different CF centers, at least one isolate from each patient at each clinical site with culture-positive patients was examined by RAPD-PCR. For neither organism were there instances of shared genotypes among different centers.
To investigate the genetic relatedness among isolates from patients at a single site, those CF centers with multiple culture-positive patients were examined in more depth, examining the majority of isolates from those centers (Fig. 1). Six clinical sites with five or more S. maltophilia culture-positive patients were examined. However, because there were only three such sites for A. xylosoxidans, sites with four or more culture-positive patients were examined. Of the six sites with five or more S. maltophilia-positive patients, three had patients with shared genotypes and three had patients with unique genotypes. Of the pairs with shared genotypes, one was a sibling pair and the other two were unrelated. Of the seven centers with multiple A. xylosoxidans-positive patients, five sites had patient pairs with shared genotypes. Of these, two pairs were siblings, one pair was friends who were frequently hospitalized at the same time, and two were epidemiologically unrelated. An example of shared genotypes of A. xylosoxidans in siblings is shown in Fig. 2.
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Persistence of colonizing isolates. In an attempt to determine whether CF patients acquired a single isolate that they kept for years or were periodically recolonized, serial isolates on a subpopulation of patients who were culture-positive for each organism were examined. Patients with ten or more isolates collected over a maximum of 2 years were targeted to determine the genotypic pattern of these serial isolates.
There were 15 patients with10 S. maltophilia isolates
collected longitudinally; isolates from 12 of them were genotyped. Because of loss during archiving or failure to prime, not all isolates
could be examined for all 12 patients. The number of potential isolates
for each individual patient ranged from 10 to 21, and the actual number
of isolates genotyped ranged from 8 to 17. Five of the 12 patients had
a single genotype identified. In the other seven only two genotypes
were identified per patient. If genotypes are designated A, B, C, etc.
in the order of appearance, the pattern in four patients was ABA and
those in one patient each were AB, ABAB (Fig.
3), and ABABA. In patients in whom throat isolates were examined at some visits because of the patient's inability to expectorate, the genotypes always correlated with a sputum
isolate at a previous or subsequent visit.
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10 A. xylosoxidans
isolates collected longitudinally; isolates from 15 of them were
examined in depth. The number of potential isolates per patient ranged from 13 to 24, and the number of isolates genotyped ranged from 13 to
19. Thirteen of the fifteen patients had a single genotype identified.
The other two patients each had an ABA pattern, with a single
intervening culture with a markedly different genotype and reversion to
the original genotype in subsequent cultures.
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DISCUSSION |
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An arbitrary primed PCR typing method was used to examine the molecular epidemiology of two organisms that have recently been described as potential pathogens in patients with CF, A. xylosoxidans and S. maltophilia. This study systematically examined the relationship between genotypes of isolates from patients within a given CF center as well as between patients at different CF centers. In addition, multiple serial isolates from patients who were culture positive for up to 2 years were genotyped in an attempt to determine the course of infection. An understanding of the epidemiology of these organisms may help us better understand their role in CF lung disease.
The results of the present study demonstrate that there are multiple, unique clones of both S. maltophilia and A. xylosoxidans that can colonize CF patients. A tropism of a small number of specific clones for the CF lung, such as has been demonstrated with B. cepacia (25, 39), was not identified in this population. The diversity of genotypes seen with RAPD-PCR in the present study is consistent with the findings of nosocomial typing studies with both of these organisms. It appears that, in general, the majority of patients have unique isolates, and only occasional small clusters of indistinguishable strains have been identified (2, 15, 21, 34, 40, 44). The present results are also consistent with several smaller studies of S. maltophilia and A. xylosoxidans isolated from patients with CF (12, 28, 43). In addition, Denton et al. (10) reported that S. maltophilia isolates from the respiratory tract of patients with CF possess a genotype which is significantly distinct from strains collected from other patients or from the environment.
The issue of patient-to-patient transmissibility of these organisms was not fully elucidated in the present study. Patients from a single center occasionally shared a genotypically identical organism, and in many of those cases there was an obvious epidemiological link. This finding was similar to results with S. maltophilia reported by Demko et al. (8), suggesting that some transmission between siblings occurs. They found 10 sibling pairs (out of 40) in which both acquired S. maltophilia, but in only 5 pairs were both siblings positive at the same time. Unfortunately, those organisms were not genotyped, so it is unknown whether they represented shared isolates or concurrent acquisition of distinct strains. Using ERIC PCR, Denton et al. (10) found that a total of 33 out of 41 CF patients were colonized with unique strains of S. maltophilia and four pairs of patients shared strains. However, further investigation found no evidence of patient-to-patient transmission.
The epidemiology of A. xylosoxidans in CF patients has been less well studied. In nosocomial outbreaks, some investigations have demonstrated person-to-person or common-source infection (12, 42), and others have found strains to be unrelated (2). However, two small studies at different pediatric centers suggested little evidence of cross-infection or a common-source outbreak in CF (12, 43).
Perhaps most interestingly, the present data showed that many patients intermittently carry more than one strain of S. maltophilia. This is more reminiscent of the epidemiologic picture seen with early P. aeruginosa infection, where sequential or intermittent genotypes are identified (5). The finding that S. maltophilia was intermittently isolated from CF patients is also supported by the study by Demko et al. (8). Their data suggested that the persistence of S. maltophilia varied greatly, with 50% of the S. maltophilia-positive patients examined having only one positive culture between 1982 and 1994. Twelve percent had up to three positive cultures, with intervening negative cultures, but unfortunately, genotyping was not done on the isolates in that study. These results suggest either separate episodes of acquisition or inadequate microbiology techniques to isolate or identify the organism on intervening cultures (4).
Epidemiologic studies of serial CF isolates of A. xylosoxidans have not been performed. The present study showed a higher percentage of colonized patients with multiple isolations of A. xylosoxidans (20 of 92 [22%]) compared with S. maltophilia (15 of 183 [8%]) and far fewer patients with more than a single genotype. This suggests that either this organism may be more persistent in CF patients than S. maltophilia and P. aeruginosa or that certain organisms may have a tropism for CF airways.
The association of S. maltophilia and A. xylosoxidans with CF has been documented for almost 2 decades (3, 20). However, the role of these organisms in CF pulmonary disease is unclear. Because both these organisms are highly antibiotic resistant and can cause significant disease in non-CF patients (19, 22, 23, 27, 29, 30), there is a suggestion that they have potential for pathogenicity in CF pathogens. In a retrospective study of 211 S. maltophilia culture-positive CF patients, Demko et al. (8) found that S. maltophilia-positive patients had a lower mean percent predicted forced expired volume in one s (48.1% vs. 57.2%) and a higher proportion of concurrent P. aeruginosa colonization (84% vs. 76%). However, 2-year mortality did not appear to be related to whether patients were ever S. maltophilia positive, nor did S. maltophilia acquisition have an obvious deleterious effect on pulmonary status over the same 2 years. Similar types of studies are lacking for A. xylosoxidans. Based upon current data, it is not possible to rule out the possibility that S. maltophilia and A. xylosoxidans cause short-term mortality or that, in patients with severe disease, the presence of these resistant organisms makes management more difficult.
While the present study has done much to elucidate the epidemiology of S. maltophilia and A. xylosoxidans in patients with CF, further studies will be required to ascertain the mode of acquisition and source of the organisms. And a definitive epidemiological study that correlates the presence of S. maltophilia or A. xylosoxidans with clinical outcomes in CF will be essential to determining the pathogenicity of this organism. Finally, the present study does not provide sufficient data to definitively state whether segregation of these patients would be a beneficial infection control measure. However, the increasing prevalence of resistant gram-negative pathogens in CF patients suggests the need for caution in dealing with any multiply resistant organism.
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FOOTNOTES |
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* Corresponding author. Mailing address: Division of Infectious Disease, Children's Hospital and Regional Medical Center, 4800 Sand Point Way, N.E., CH-32, Seattle, WA 98015. Phone: (206) 526-2073. Fax: (206) 527-3890. E-mail: jburns{at}chmc.org.
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Journal of Clinical Microbiology, October 2001, p. 3597-3602, Vol. 39, No. 10
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.10.3597-3602.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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