• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of cmrPermissionsJournals.ASM.orgJournalCMR ArticleJournal InfoAuthorsReviewers
Clin Microbiol Rev. Jan 1998; 11(1): 57–80.
PMCID: PMC121376

Microbiological and Clinical Aspects of Infection Associated with Stenotrophomonas maltophilia

Abstract

The gram-negative bacterium Stenotrophomonas maltophilia is increasingly recognized as an important cause of nosocomial infection. Infection occurs principally, but not exclusively, in debilitated and immunosuppressed individuals. Management of S. maltophilia-associated infection is problematic because many strains of the bacterium manifest resistance to multiple antibiotics. These difficulties are compounded by methodological problems in in vitro susceptibility testing for which there are, as yet, no formal guidelines. Despite its acknowledged importance as a nosocomial pathogen, little is known of the epidemiology of S. maltophilia, and although it is considered an environmental bacterium, its sources and reservoirs are often not readily apparent. Molecular typing systems may contribute to our knowledge of the epidemiology of S. maltophilia infection, thus allowing the development of strategies to interrupt the transmission of the bacterium in the hospital setting. Even less is known of pathogenic mechanisms and putative virulence factors involved in the natural history of S. maltophilia infection and this, coupled with difficulties in distinguishing colonization from true infection, has fostered the view that the bacterium is essentially nonpathogenic. This article aims to review the current taxonomic status of S. maltophilia, and it discusses the laboratory identification of the bacterium. The epidemiology of the organism is considered with particular reference to nosocomial outbreaks, several of which have been investigated by molecular typing techniques. Risk factors for acquisition of the bacterium are also reviewed, and the ever-expanding spectrum of clinical syndromes associated with S. maltophilia is surveyed. Antimicrobial resistance mechanisms, pitfalls in in vitro susceptibility testing, and therapy of S. maltophilia infections are also discussed.

Following a lengthy period of uncertain taxonomic status, the nonfermentative gram-negative bacillus previously known as Pseudomonas maltophilia or Xanthomonas maltophilia has now been reclassified as Stenotrophomonas maltophilia, the sole member of the genus Stenotrophomonas. Despite reports in the earlier literature that the bacterium was of strictly limited pathogenicity, S. maltophilia has risen to prominence over the last decade as an important nosocomial pathogen associated with significant case/fatality ratios in certain patient populations, particularly in individuals who are severely debilitated or immunosuppressed. The spectrum of clinical syndromes associated with S. maltophilia infection continues to expand. Despite this, little is known about virulence factors associated with the bacterium. In addition, there is still considerable uncertainty about the route(s) of acquisition of S. maltophilia. Although a number of sources in the hospital environment have been identified, strains isolated from these sites often differ from those obtained from clinical material. In addition, evidence from a small number of reported outbreaks indicates that person-to-person transmission may be an infrequent occurrence in the nosocomial setting.

The majority of strains of S. maltophilia are characterized by their resistance to many currently available broad-spectrum antimicrobial agents, including those of the carbapenem class. Although resistance to drugs of the β-lactam class has been extensively investigated, mechanisms which confer resistance to other agents have received comparatively little attention. Current methods of in vitro susceptibility testing manifest significant variations in observed results hampering the selection of optimal therapy for S. maltophilia-associated infection.

Moreover, in vitro susceptibility data frequently do not correlate with a successful clinical outcome. Management of infection is sometimes further complicated by the emergence of mutants exhibiting pleiotropic resistance. Accordingly, attempts have been made to identify combinations of antimicrobial agents which exhibit in vitro synergy against S. maltophilia and which may also prevent the emergence of resistance. Although some of these combinations appear promising in this respect they remain largely untested in the clinical setting.

MICROBIOLOGY

Taxonomy

S. maltophilia is the only member of the genus Stenotrophomonas (Stenos, Greek: narrow; trophos, Greek: one who feeds; monas, Greek: a unit, monad; i.e., a unit feeding on few substrates; and malt, Old English: malt; philos, Greek: friend; i.e., a friend of malt). The genus was proposed in 1993 by Palleroni and Bradbury (313) after many years of debate regarding the appropriate taxonomic position of this organism. The type strain was isolated in 1958 by Hugh from an oropharyngeal swab from a patient with an oral carcinoma (184) and named Pseudomonas maltophilia (185, 186). Subsequently, Hugh and Ryschenkow reclassified “Bacterium bookeri,” which had been isolated from pleural fluid in 1943 by J. L. Edwards, as P. maltophilia (184). Pseudomonas melanogena isolated from Japanese rice paddies in 1963 was later recognized as Pseudomonas maltophilia (235), as were strains which had initially been characterized as Pseudomonas alcaligenes by Komagata (184, 234). Similarly, strains of Alcaligenes faecalis as described by Ulrich and Needham (418) were subsequently reclassified by Hugh and Ryschenkow (186) as P. maltophilia. Later, the use of DNA-rRNA hybridization techniques revealed the presence of five rRNA homology groups in the genus Pseudomonas, as it then was, and showed that the rRNA cistrons of the P. maltophilia type strain ATCC 13637 were most similar to those of three strains of Xanthomonas (314).

This information was used by Swings et al. in 1981 to propose that P. maltophilia be reclassified in the genus Xanthomonas as X. maltophilia (402). In addition, they cited several other factors to support their case. These included the guanine-plus-cytosine (G+C) content (P. maltophilia, 63 to 67.5%; Xanthomonas, 63 to 70%); comparative enzymology, particularly the absence of NADP-linked dehydrogenases; the occurrence of the same type of ubiquinones (P. maltophilia and Xanthomonas spp. both possess ubiquinones with eight isoprene units, whereas all other Pseudomonas strains possess nine units); and similar cellular fatty acid composition. A subsequent analysis of whole-cell proteins patterns (424) appeared to support this proposal. Additional evidence from isoelectric focusing studies of outer membrane esterase (87) confirmed that P. betle and P. hibiscicola were synonyms of X. maltophilia (383, 421). However, the proposed reclassification of P. maltophilia as X. maltophilia did not meet with universal approval (312), and the controversy about the taxonomic status of this bacterium in the genus Xanthomonas remained unresolved (53).

The controversy was partly because some of the evidence put forward by Swings et al. (402) was subsequently contradicted by the findings of later studies. During an extensive DNA-rRNA hybridization study of the genus Pseudomonas, different melting temperatures were reported for the same 27 strains of Xanthomonas used in the proposal of Swings et al., despite the use of identical experimental conditions and the same X. campestris type strain as reference rRNA (96). The range for X. maltophilia was 76.5 to 78°C, almost overlapping the range for the genus Xanthomonas reported by Swings et al. (78.8 to 81.5°C) but further removed from that (80.0 to 81.5°C) reported later by De Vos and De Ley (96). In addition, Yang et al., using polyamine and fatty acid analysis (460, 461), demonstrated that X. maltophilia possessed profiles distinct from other species within the genus Xanthomonas. Furthermore, the possession of ubiquinones with eight isoprene units was shown not to be limited to X. maltophilia and other members of the genus Xanthomonas by Oyiazu and Komagata, who cited that they were found in several other pseudomonads including P. avenae and P. palleroni of rRNA group III (311).

These factors, along with supplementary evidence, were used to request a reinterpretation of the taxonomic position of X. maltophilia (425). This was supported by experiments with a Xanthomonas-specific 16S rDNA sequence as the primer for PCR (254). Xanthomonads were recognized by the presence of a single 480-bp PCR fragment; however, X. maltophilia strains produced additional PCR fragments, leading the author to conclude that X. maltophilia does not belong in the genus Xanthomonas.

Continuing dissatisfaction with the classification of this organism finally gave rise to the proposal in 1993 to create the new genus Stenotrophomonas with S. maltophilia as the sole member (313). More recently, Nesme et al. confirmed the distinction between S. maltophilia and members of the genus Xanthomonas by using restriction mapping of PCR-amplified 16S rRNA genes (293).

Recently, Drancourt et al. proposed a new species; Stenotrophomonas africana, which is biochemically identical to S. maltophilia except for its inability to assimilate cis-aconitate. Genotypic analysis, however, revealed only 35% DNA homology between the two species (104).

Morphology, Culture Characteristics, and Growth Requirements

Cells of S. maltophilia are straight or slightly curved nonsporulating gram-negative bacilli that are 0.5 to 1.5 μm long. They occur singly or in pairs and do not accumulate poly-β-hydroxybutyrate as intracellular granules. They are motile by means of several polar flagella. The colonies are smooth, glistening, with entire margins and are white to pale yellow. Although Nord et al. (298) observed beta-hemolysis in 11 of 31 strains they examined, the bacterium is not generally considered to be beta-hemolytic. However, on blood agar there may be a greenish discoloration of the medium around confluent growth (149). On clear media, some strains may exhibit a brownish discoloration. This phenomenon has been attributed to a secondary chemical reaction among extracellular products and is more intense when these strains are incubated at 42°C (183) or cultured on media with a high tyrosine content (41).

S. maltophilia is an obligate aerobe. Growth does not occur at temperatures lower than 5°C or higher than 40°C and is optimal at 35°C. Margesin and Schinner reported the isolation from an alpine environment of a strain of the bacterium which was capable of growth at 10°C (258). Methionine or cystine is required for growth by most but not all strains (193, 260).

Biochemical Characteristics

The bacterium has been regarded as relatively metabolically inactive (395), but a variety of unusual substrates, including the aminoglycoside antibiotic streptomycin (127), may be metabolized (37, 39, 55, 191, 209, 244, 273, 291, 333, 398) and strains of the bacterium have been investigated for their potential use as biodegradative agents. Selected biochemical characteristics and microbiological reactions of S. maltophilia are shown in Table Table1.1.

TABLE 1
Biochemical and other characteristics of S. maltophilia

Cellular Constituents and Antigenic Structure

Somatic O antigens and flagellar H antigens have been described (186). A total of 31 O antigens have been identified, and these have been used to type S. maltophilia in epidemiological studies (220, 374, 375). The structures of seven of these antigens, including O3, which represents the most frequently occurring serotype, have been determined (98, 292, 448452). The repeating units of these antigens are all branched and contain between three and five saccharides including relatively uncommon moieties such as 6-deoxy-l-talose, 3-acetamido-3,6-dideoxy-d-galactose, and 4-acetamido-4,6-dideoxy-d-mannose. Cross-reactions with the O antigens of S. maltophilia and Brucella spp. have been reported (76). Cross-reactions with Renibacterium salmoninarum have also been observed (18, 57), and Orrison et al. reported nonreciprocal cross-reactivity between Legionella pneumophila and S. maltophilia (309). Preparations of the bacterium are also capable of agglutinating mouse, rabbit, and human spermatozoa (26).

Moss et al. investigated the cellular fatty acid composition of S. maltophilia and identified the presence of relatively large amounts (26% of the total) of a branched-chain 15-carbon fatty acid:13-methyltetradecanoic acid (282). In addition, they identified three additional branched-chain hydroxy-fatty acids, i.e., 2-hydroxy-9-methyldecanoic, 3-hydroxy-9-methyldecanoic, and 3-hydroxy-11-methyldodecanoic acids, which they did not detect in a range of other bacteria examined (281). They suggested that the uniqueness of the fatty acid profile of S. maltophilia could be of value in the identification of the bacterium.

Genetics

Little is known of the genetic structure of S. maltophilia. A gene of 1,362 bp encoding a 48.5-kDa chorionic gonadotrophin-like hormone has been sequenced (164, 166). This hormone bears an immunological resemblance to human chorionic gonadotrophin (hCG) (163, 165) (see below). The gene encoding the L1 β-lactamase of S. maltophilia (blaS) was cloned and expressed in Escherichia coli by Dufresne et al. (106) and has been sequenced by Walsh et al. (439). Very recently, the same group published the sequence of the L2 β-lactamase (440). The sequences of the alkA and alkB genes, which code for alkane hydroxylase and rubredoxin reductase, respectively, have also been determined (245). Of 18 strains of S. maltophilia analyzed in one study, 5 were shown to harbor plasmids (380), but further analysis was limited.

Habitat

S. maltophilia is found in a wide variety of environments and geographical regions, including Antarctica (430), and occupies ecological niches both inside and outside hospitals. It has been isolated from a number of water sources including rivers, wells, a hypereutrophic lake, and bottled water (in which it may be responsible for altered organoleptic properties), and sewage (13, 167, 176, 183, 184, 185, 219, 288, 319). The bacterium has also been recovered from a variety of soil (44, 85, 127, 400) and plant rhizosphere environments, including grasses, sugarcane and palms (202), from wheat (203), cabbage, rape, mustard, corn (86), beet (86, 243), bananas, cotton, beans, tobacco (183), rice paddies (235), citrus plants (1), orchids (447), irises (25), legume inoculants which use nonsterile peat as a carrier (306), and stored timber (108). Iizuka and Komagata reported the isolation of S. maltophilia from oil brines and other related materials from oil fields in Japan (191). S. maltophilia will also grow on loofah sponges (51).

The potential use of S. maltophilia as a biological control agent in rhizosphere environments and against agricultural pests has been explored (31, 32, 112, 173, 232, 239, 242, 264, 382). Given the broad range of phytopathogenic fungi inhibited by the bacterium, it is not altogether surprising that S. maltophilia has recently been reported to inhibit the growth of human fungal pathogens such as Candida spp. and Aspergillus fumigatus (213). The proposal that the observed inhibition is due to pyrrolnitrin production (213) merits further investigation, although it has also been suggested that chitinolytic activity exhibited by the bacterium may be of importance in this respect (232). Recently, Jakobi et al. reported the production of maltophilin, a novel macrocyclic lactam agent with anti-fungal activity against saprophytic, phytopathogenic, and human isolates, by S. maltophilia (195). Food sources for the bacterium include frozen fish (186), milk (185, 201), poultry eggs (7, 469), and lamb carcasses (381). In the laboratory, the organism has been isolated from contaminated cell cultures (395) and an isolate of S. maltophilia contaminating Sephadex columns was reported to tolerate 1% sodium azide (48).

The bacterium has also been isolated from a wide range of nosocomial sources, which are listed in Table Table2.2.

TABLE 2
Nosocomial sources of S. maltophilia

The possibility of S. maltophilia being found in the domestic setting, in contrast to hospitals, has received comparatively little attention. In their investigation of the prevalence of pseudomonads in the domestic environment of cystic fibrosis sufferers and of control families, Mortensen et al. recorded low rates of isolation (4 of 407 cultures) of S. maltophilia, although it should be noted that they did not use a selective medium specifically intended to recover this bacterium (280). This is significant, because isolation from environmental samples and other heavily contaminated materials can be enhanced by the use of selective media (44, 202, 216).

Although relatively little information is available on the ability of S. maltophilia to survive drying, Rosenthal reported that whereas the bacterium was frequently isolated from wet environments such as sink traps, recovery from dry sites such as hospital floors was very uncommon (363). This is in agreement with the findings of Moffet and Williams (274), who cultured S. maltophilia from various nosocomial water samples but noted that isolation of the bacterium from dry surfaces of respiratory therapy equipment was comparatively rare. Hirai (177) investigated the ability of a single clinical strain of S. maltophilia to survive when inoculated onto cotton lint and glass plates. On the former, viable bacteria could not be identified 7 h after inoculation; whereas on the latter, viable organisms were recovered after the same period of incubation although less than 1% of the initial inoculum survived. The D value (the time required for 90% reduction of the initial inoculum) for survival on glass plates was 2.4 h. Although the presence of proteins, such as bovine serum albumin, increased the survival of other gram-negative bacteria, this was not observed with S. maltophilia (177).

Human Carriage

Few studies have investigated the carriage rate of S. maltophilia in humans. Isolation from feces was first reported by Hugh and Ryschenkow in 1961 (186). Using a selective medium, von Graevenitz and Bucher recorded a fecal carriage rate of 10.9% (14 of 128 samples) in outpatients with diarrheal illness or their contacts (436). Rosenthal, however, was unable to isolate S. maltophilia from the rectal swabs of 50 ambulatory nursing home patients (363), although it should be noted that their isolation medium was of poorer selectivity than the medium of von Graevenitz and Bucher.

In a small series of 12 patients with hematologic malignancy, Kerr et al. (215) reported a fecal carriage rate of 33%. In contrast, only 2 of 69 (2.9%) subjects in a control group were fecal excreters of S. maltophilia. There have been few systematic studies of carriage rates at sites other than the lower gastrointestinal tract. Although carriage on the hands of health care workers during nosocomial outbreaks of S. maltophilia infection has been noted (419, 433), Khardori et al. (220) were unable to isolate the bacterium from skin swabs taken from hospital personnel. S. maltophilia has been isolated from the oropharyngeal swabs of healthy adults (183), although another study examining 200 throat or pharyngeal washings from healthy individuals participating in a health-screening program did not reveal the presence of the bacterium in any sample (363). Similarly throat swabs from hospital staff taken during the investigation of the nosocomial outbreak, reported by Khardori and colleagues, did not yield the bacterium (220). Respiratory tract carriage rates in individuals with cystic fibrosis are discussed in the section on respiratory tract infection, below. Carriage rates of 0% were recorded for 50 skin swabs of patients attending a cancer-screening clinic and for 50 vaginal swabs taken from gynecology clinic attendees (363).

Even less is known about animal sources of S. maltophilia. The bacterium has been isolated from fish, raw cows’ and ewes’ milk, rabbit feces (186, 248), lizards, frogs (183), the mouths and cloacae of captive snakes (105), and the gastrointestinal tracts of laboratory animals (135, 410). The bacterium has also been implicated in fleece rot of sheep (253). Lysenko and Weiser reported the recovery of S. maltophilia from the nematode Neoaplectana carpocapsae (252).

Following the isolation of S. maltophilia from the ovarian fluid of a sow, Richert and Ryan (353) and others (2) demonstrated that the bacterium was capable of binding hCG. Subsequently, it was shown that an hCG-like protein (xCG) from S. maltophilia has a high degree of homology with the β subunit of hCG (164). An autocrine and/or paracrine function for xCG has been suggested following observations that when added to growth media, it (and hCG) causes changes in both the cell growth cycle and bacterial morphology (65). The nucleotide sequence of the chorionic gonadotropin-like protein receptor has been published (164, 166).

Virulence Factors

Little is known of the putative virulence factors of S. maltophilia. The failure to distinguish between colonization and infection has fostered the belief that S. maltophilia is an organism of very limited pathogenicity. These views may have been reinforced by studies in which cases of infection with the bacterium were not associated with an unfavorable clinical outcome. For example, in their review of 106 intensive care unit patients infected or colonized with the bacterium, Villarino et al. were unable to attribute the death of any patient directly to S. maltophilia infection (433). Gardner et al. (145) suggested that S. maltophilia was often associated with clinically overt infection only when acting synergistically with other pathogens. Early attempts to induce infection in an experimental animal model appeared to support the hypothesis that S. maltophilia does not cause serious sepsis when whole bacteria are administered intravenously to mice.

Although extracts of bacterial cultures were associated with some toxicity, it was less severe than that in similar preparations of strains of E. coli (160). Elaboration of a range of extracellular enzymes by S. maltophilia, including DNase, RNase, fibrinolysin, lipases, hyaluronidase, protease, and elastase, was described in several early reports (9, 42, 43, 52, 196, 298, 302, 303, 377), and Bottone et al. have proposed that these enzymes may play a role in the pathogenesis of S. maltophilia-associated infection (52). They reported a case of ecthyma gangrenosum in a leukemic patient with S. maltophilia bacteremia. Because bacterial production of protease and elastase is deemed important in the pathogenesis of cases of ecthyma gangrenosum associated with P. aeruginosa septicemia, they examined the S. maltophilia isolate for elaboration of these enzymes and found that it was an “avid protease and elastase producer” (52). A larger study of 52 strains of clinical and environmental origin examined the production of nine extracellular enzymes. No strain produced lecithinase, hyaluronidase, or chondroitin sulfatase, whereas all the strains produced protease and elastase. Elastase production was variable, but there was no significant difference between clinical and environmental strains. Although DNase, lipase, and fibrinolysin were produced by all strains at 20°C, clinical isolates were significantly more likely to produce these enzymes when grown at 37°C (409).

Adherence to plastic is considered an important property of bacteria commonly implicated in line-related colonization and infection, and strains of S. maltophilia of both clinical and environmental origin have been reported to adhere to several types of plastic materials including intravenous cannulae (214).

Recently Jucker et al. investigated the adherence of a strain of S. maltophilia to both glass and Teflon (200). They noted that adhesion to these negatively charged materials was promoted considerably by the positive charge manifested by this strain at physiologic pH.

The ability of S. maltophilia to survive and multiply within total parenteral nutrition and other types of intravenous infusates may also contribute to the pathogenesis of intravenous line-related infections (266, 323). Similarly, the ability of this bacterium to grow in dialysis fluids with the release of low-molecular-weight pyrogens, which are apparently different from endotoxin-like moieties as detected in the Limulus amebocyte lysate assay, may be important in the pathogenesis of pyrogenic reactions during hemodialysis (138).

The role of a cell wall-associated immunoglobulin G binding protein in the pathogenesis of S. maltophilia infection (162) requires further investigation. Serum resistance is a phenomenon frequently exhibited by gram-negative bacteria associated with septicemia, and a study of a small number of strains of S. maltophilia noted that clinical isolates were much more likely to exhibit this property than were environmental isolates (217).

Virulence factors of importance in the pathogenesis of S. maltophilia-associated pulmonary infection remain to be characterized. Grant et al. (158) were unable to demonstrate adherence of the bacterium to cultured hamster tracheal cells.

Laboratory Isolation

S. maltophilia can be isolated quite readily from normally sterile sites on a wide range of commonly used solid media, including blood, heated blood, MacConkey, and cysteine lactose electrolyte-deficient agars. It will grow overnight at temperatures ranging from 20 to 37°C in air and will also grow in 5% CO2. Most blood culture systems are capable of growing S. maltophilia with various degrees of efficiency. Published evaluations are summarized in Table Table3.3.

TABLE 3
Isolation of S. maltophilia by blood culture systems

It is difficult to determine the relative merits of the various systems with respect to isolation of S. maltophilia because of the small numbers of strains in many studies. It should be noted, however, that S. maltophilia has been isolated from terminal subcultures (false negative) taken from a number of systems including Oxoid Signal (396), BACTEC NR 660 (297), BacT/Alert (357), and Difco ESP (278), although on most occasions other bottles within each set were positive. In one study, the Isolator system detected significantly more positive cultures (P < 0.01) and more sepsis episodes (P < 0.02) with S. maltophilia than did aerobic bottles of the Difco ESP system (227).

Selective Media

A number of selective media have been developed for the isolation of S. maltophilia from clinical or environmental specimens likely to be contaminated with other bacteria. Early examples, such as mineral acetate lactate methionine agar were of relatively poor selectivity (363). Antimicrobial agents were added to later medium formulations in an attempt to improve this. Juhnke and Des Jardins developed Xanthomonas maltophilia selective medium for the isolation of S. maltophilia from soil and rhizosphere environments (202). This medium contains six antibacterial agents, i.e., cephalexin, bacitracin, penicillin G, novobiocin, neomycin, and tobramycin, and two antifungal agents, i.e., nystatin and cycloheximide. Maltose and bromothymol blue were also included to facilitate the identification of S. maltophilia colonies, which, because of acid production from maltose, appear as orange with a yellow halo (202). In an investigation into environmental reservoirs and hand carriage of S. maltophilia by health care personnel, Villarino et al. used tryptic soy agar supplemented with 5% sheep blood to which 5 μg of gentamicin per ml had been added, although no comparator medium was tested (433).

Several media which take advantage of the inherent resistance of S. maltophilia to carbapenems have also been developed. Imipenem added to blood or MacConkey agar has been used to isolate S. maltophilia from stool (436) and sputum (154) samples. MacConkey agar which incorporated imipenem at a concentration of 10 μg/ml was more inhibitory for some strains than was imipenem-blood agar (436). Khardori et al. (220) used MacConkey agar supplemented with 25 μg of imipenem per ml, which might have contributed to the low rate of isolation of S. maltophilia from environmental sources during their investigation of a nosocomial outbreak. The imipenem-containing medium of Bollet et al. (44) incorporates methionine, thus taking advantage of the requirement of most strains of the bacterium for this amino acid (193, 260). Media which contain imipenem as the sole selective agent may fail to inhibit the growth of some organisms found in stool cultures, particularly Enterococcus faecium and Candida spp. These problems can be circumvented by the further addition of vancomycin and amphotericin B to imipenem-containing agar (216) and the use of a mannitol-bromothymol blue indicator system to facilitate the differentiation of S. maltophilia (which does not produce acid from mannitol) from other imipenem-resistant gram-negative bacteria. This medium was shown to enhance the isolation of S. maltophilia from sputum samples taken from patients with cystic fibrosis (92) and the feces of patients with hematological malignancy (216).

Identification in the Clinical Laboratory

S. maltophilia can be identified in the clinical laboratory by standard biochemical and other tests (151) (Table (Table1).1). In addition, Townsend et al. suggested that in vitro synergism between aztreonam and clavulanic acid by using disks containing 30 and 10 μg of drug, respectively, can be used in the presumptive identification of the bacterium (412). Furthermore, several commercial products which are intended to aid in the identification of gram-negative non-fermentative rods have been tested for their ability to accurately identify S. maltophilia (19, 70, 110, 205, 228, 229, 263, 271, 304, 332, 352, 356, 385, 387, 394, 407, 435, 441). Details of studies which have examined the utility of these methods, including automated and semiautomated systems, for the identification of this bacterium are listed in Table Table4.4.

TABLE 4
Commercial systems used to identify S. maltophilia

The limited number of S. maltophilia strains used in many of these evaluations (e.g., the study of Varettas et al., in which a single strain was used [426]), however, precludes definitive conclusions about the relative abilities of each system with respect to correct identification of this particular organism. Where comparative studies have evaluated automated and nonautomated systems, there have been no significant differences in their ability to identify S. maltophilia (304, 356).

Given its erstwhile relative infrequency of isolation from clinical material and uncertain taxonomic status, it is perhaps not surprising that several early reports noted that the identity of S. maltophilia could be confused with that of other bacteria and that it had been misidentified as Pseudomonas alcaligenes (192), Bordetella bronchiseptica, and Alcaligenes faecalis (186). Later reports, however, emphasize that misidentifications still occur. One strain of Pseudomonas stutzeri was misidentified as S. maltophilia by the Radiometer Sensititre AP80 (394), an isolate belonging to Flavobacterium group IIB was misidentified by the Vitek AutoMicrobic system (385), and two isolates were misidentified as Pseudomonas diminuta by the PASCO MIC-ID system (352).

Misidentification of S. maltophilia can have important clinical and psychosocial implications. In a survey of 32 “Burkholderia cepacia” strains isolated from cystic fibrosis patients sent to the Canadian Pseudomonas Repository Laboratory, 3 were subsequently identified as S. maltophilia (59). Misidentifications of this type are of particular concern since 20% of cystic fibrosis patients colonized with B. cepacia are known to suffer a syndrome of pneumonitis, septicemia, and rapid clinical deterioration and thus its isolation is understandably viewed with great alarm by these patients and their care givers.

Conversely, some systems have misidentified other organisms as S. maltophilia. In an evaluation of the RapID NF Plus, one strain of B. cepacia needed additional biochemical tests before it could be correctly distinguished from S. maltophilia (229). In addition to methods which rely on the biochemical reactions for the identification of S. maltophilia, several other techniques have undergone evaluation. These include gas-liquid chromatography (240), direct-probe mass spectrometry (343), and molecular methods. Zechman and Labows (468) used automated headspace concentration gas chromatography to identify S. maltophilia and were able to distinguish the bacterium from P. aeruginosa, B. cepacia, P. fluorescens, and P. putida. Veys et al. correctly identified 59 strains of S. maltophilia by the presence of three characteristic peaks consisting of 3-hydroxydodecanoate, 13-methyltetradecanoate, and 12-methyltetradecanoate (431). An automated gas-liquid chromatography system, the Microbial Identification System (Microbial ID, Newark, Del.), correctly identified 45 of 47 (96%) S. maltophilia strains tested, with the others being misidentified as Xanthomonas campestris (310).

Molecular methods for the identification of S. maltophilia have, to date, received comparatively little attention. By using single-strand conformation polymorphism electrophoresis of PCR-amplified 16S rRNA fragments, species-specific patterns for S. maltophilia have been observed (445). Tyler et al. (417) were able to distinguish between S. maltophilia and seven species of Pseudomonas by identifying differences in the sequences of 16S to 23S rDNA internal transcribed spacers.

EPIDEMIOLOGY

Until relatively recently, S. maltophilia was considered an unusual organism to isolate in the diagnostic microbiology laboratory, despite earlier claims that it was the second most common nonfermentative gram-negative bacillus (after P. aeruginosa) isolated from clinical specimens (41, 157, 180, 363). Isolation rates have been increasing since the early 1970s. At the M. D. Anderson Cancer Center (Houston, Tex.), the rate of S. maltophilia isolations per 10,000 admissions rose from less than 2 in 1972 to 8 in 1984 (115), and in 1993 at that institution, the bacterium represented the fourth most common gram-negative pathogen recovered from clinical specimens (428). The annual isolation rate at the University of Virginia Hospital doubled from 7.1 to 14.1 per 10,000 patient discharges from 1981 to 1984 (279), and at the Mayo Clinic, the incidence rose from 12.8 in 1984 to 37.7 per 10,000 patient discharges in 1987 (262). At a 470-bed tertiary trauma referral hospital affiliated with the University of Utah School of Medicine (Salt Lake City, Utah), the median monthly rate of S. maltophilia infection and/or colonization from January 1988 to February 1989 was significantly higher than for January through December 1987 (18.3 versus 7.4 per 1,000 patient-days; P < 0.0001) (433), although this rise was due in part to an epidemic on the shock-trauma intensive care unit during the former period. One report suggests that isolations have continued to rise in the 1990s: in a French hospital, there were 20 isolates of S. maltophilia in 1991, 24 in 1992, and 65 in 1993 (84). Given that advances in medical technology are likely to create an increased population of individuals with risk factors which predispose them to infection, the incidence of S. maltophilia infection is likely to increase (285). These risk factors are summarized in Table Table5.5.

TABLE 5
Risk factors associated with S. maltophilia infection

Detailed comparisons between studies which have analyzed predisposing factors are not possible for a number of reasons. These include variations in patient mix, criteria used to define infection, and statistical methods used to analyze data. It is noteworthy, however, that several of these—such as prior exposure to antimicrobial agents—have been consistently associated with S. maltophilia infection and that nearly all of them are indicative of patient debilitation. Nagai (287) noted that 39 of 82 (48%) patients from whom S. maltophilia was cultured had a neoplastic lesion at the site of isolation of the bacterium. He proposed that an altered microenvironment caused by anaerobic glycolysis in neoplastic tissue could provide conditions favorable for the multiplication of certain microorganisms and went on to suggest that S. maltophilia infection in a patient without other predisposing factors should prompt the diagnostic possibility of an associated malignant lesion (287).

Although antecedent therapy with carbapenems, to which the bacterium is inherently resistant, has been cited by several authors as a risk factor (21, 56, 60, 97, 99, 107, 116, 139, 189, 414, 453), it is not a prerequisite for colonization or infection. Indeed, other investigators have highlighted many cases of S. maltophilia infection where patients had received broad-spectrum antibiotics other than imipenem, such as aminoglycosides, fluoroquinolones, and extended-spectrum cephalosporins (63, 187, 218, 241). Vartivarian et al., in a review of 114 patients with mucocutaneous and soft tissue infection, found no preponderance of infection in patients receiving imipenem (429). Similarly, in their series of isolates from lower respiratory tract specimens of 27 patients in intensive care units, Maningo and Watanakunakorn noted that although most of the patients had received multiple antimicrobial agents before S. maltophilia isolation, only 2 had received imipenem (257). Heath and Currie (172), in their series of S. maltophilia infections from tropical Australia, observed a marked seasonal variation, with the peak in incidence occurring in the wet season. They postulated that this may follow an increased usage of ceftazidime and imipenem as therapy for Burkholderia pseudomallei and Acinetobacter baumanii infections, which are also more common at this time. This interesting hypothesis warrants further investigation.

Several nosocomial outbreaks of S. maltophilia infection and/or colonization have now been described (36, 61, 67, 84, 128, 130, 147, 220, 241, 308, 342, 369, 416, 419, 422, 433, 455, 462). In several instances, putative environmental reservoirs for the bacterium have been identified. Contaminated deionized water used to make up disinfectant was found to be the source of one S. maltophilia outbreak which involved 63 patients in an Australian hospital (455). Four cases of septicemia with S. maltophilia were attributed to inadequate disinfection of reusable capillary dialyzers (422). Dialyzer effluents were contaminated with >104 CFU of S. maltophilia per ml and had extremely low formaldehyde concentrations of between 0.0014 to 0.005% (against the expected 4%). Eight patients (four with leukemia, four with multiple myeloma) on a hematology ward developed infection with S. maltophilia, whose source was traced to an ice-making machine (342). The ice was used for making cold drinks and contained high levels of S. maltophilia (>105 CFU/ml).

Typing Schemes

A variety of typing schemes have been developed in an attempt to elucidate the epidemiology of infections caused by S. maltophilia, and they have been used, with various degrees of success, to investigate nosocomial outbreaks. Phenotypic methods include serotyping based on heat-stable O antigens (220, 374, 375, 433) and lipopolysaccharide typing (12).

Typing based on comparison of antibiograms is of limited applicability because of a lack of variation in resistance patterns expressed by most strains (419). Similarly, biotyping is poorly discriminative because of a paucity of interstrain variability manifested by the bacterium. More recently, genotypic typing techniques have been the subject of much attention. Methods evaluated have included ribotyping (36, 114, 147), pulsed-field gel electrophoresis (PFGE) (241, 369, 405, 419, 462), random amplification of polymorphic DNA (RAPD) (67, 84, 419, 462), and enterobacterial repetitive intergenic consensus PCR (ERIC-PCR) (67). Other techniques which have been used to study the epidemiology of S. maltophilia are pyrolysis mass spectrometry (308) and multilocus enzyme electrophoresis (376).

An outbreak involving 45 patients on a shock-trauma intensive care unit was investigated by serotyping (433). Of 22 patient isolates available for typing, 19 (86%) were of serotype 10. A total of 11 of 17 samples from inanimate environmental sites (including respirometers, a tracheal suction catheter, components of a ventilation circuit, and water from a sink) and 3 of 6 hand cultures from nurses and respiratory therapists were positive for S. maltophilia. Of these 14 isolates, 13 were also of serotype 10. Reemphasis of the importance of hand washing before and after all patient contact, implementation of secretion and drainage precautions for all patients with S. maltophilia would infection, the use of gloves when suctioning or manipulating the respiratory tracts of ventilated patients, and high-level disinfection of respirometers between use in different patients were the measures used to successfully bring an end to the outbreak.

Serotyping was also used to analyze 52 clinical isolates collected from 35 cancer patients over a 6-month period (220). Again, serotype 10 was the most common type (16 of 52 isolates [31%]). Eight other types were found among the remaining 36 isolates. Three environmental isolates were found on the medical intensive care unit, two of which were from water faucets and one was from a water sample. One of these belonged to serotype 10. The number of S. maltophilia isolates decreased following the earlier introduction of appropriate antibiotic therapy for S. maltophilia infection and an increase in the temperature of the boiler for hot water from 40 to 43.3°C. In a more recent study, Schable et al. examined 900 isolates from 10 countries and noted that 795 (88.3%) were serotypable. The most common serotypes were 10, 3, and 19 respectively, and they were predominantly associated with respiratory and blood isolates (375). This typing system is, however, of limited applicability because reagents are not widely available and because, as shown in the study of Schable et al., more than 10% of isolates are untypable. In addition, this method appears less discriminatory than other techniques (376).

The technique of pyrolysis mass spectrometry relies on the analysis of the products of thermal degradation of materials (337). It was used to investigate a suspected outbreak of S. maltophilia cross-infection and colonization on a heart-lung transplant intensive care unit (308). The respiratory tracts of five patients became colonized or infected over a 19-day period. All five had been nursed in either of two single cubicles equipped with positive-pressure ventilation. Extensive environmental sampling failed to reveal a source of S. maltophilia, although unauthorized reuse of “single-use” disposable nebulizers was uncovered. These had been cleaned but not resterilized. Twelve “cleaned” nebulizers were sampled prior to their intended reuse, and S. maltophilia was cultured from one of them. Although the five patient strains and the nebulizer strain were all different, the authors considered the outbreak to be related to reuse of disposable nebulizers, and the outbreak ceased when this practice was terminated.

Ribotyping has been used in the investigation of cases of nosocomial S. maltophilia bacteremia which occurred over 13 months in seven patients residing on four different wards of a pediatric hospital (36). Four patients (three on a gastroenterology ward, one on the intensive care unit) had the same ribotype, although the mode of transmission between these patients was not readily apparent. Ribotyping was also used to characterize 77 consecutive clinical S. maltophilia isolates in a Danish hospital (147). Great diversity was found among the ribotypes of the hospital strains, and no single-strain outbreak was detected. Potential reservoirs for these strains were not determined. Wust et al. (458) used ribotyping to demonstrate that increasing antimicrobial resistance in serial isolates of S. maltophilia from a patient with cystic fibrosis was due to acquisition of resistance by the original strain rather than infection by other strains.

Several reports evaluating the usefulness of PFGE have been published. Thirty S. maltophilia strains from three countries (Brazil, Switzerland, and the United States) were analyzed by PFGE of XbaI or SpeI digests (369). With the exception of four strains from Brazil collected during an outbreak on a dialysis unit, all the strains were unrelated. Additional details relating to the Brazilian outbreak were, unfortunately, not given.

Ten strains from five patients and two environmental strains relating to a S. maltophilia outbreak on a hematology unit were examined by PFGE following chromosomal DNA digestion with DraI (405). The five patients each had unique strains; however, the environmental isolates, one from a kitchen water faucet and one from a shower head, each matched the profile of one of the patient isolates.

PFGE following DraI digestion was also used to analyze 109 clinical strains collected over a 10-month period in a Canadian hospital (462). This revealed 62 unique DNA restriction profiles. Respectively, 23, 11, 6, 6, and 3 strains had concordant profiles in each of five types. Four profiles were seen among 8 strains (2 strains with each profile), and the remaining 52 strains had unique profiles. Two profiles accounted for 32 (61.5%) of the 52 isolates from the intensive care units but only for 2 of 31 ward isolates. This was suggestive of nosocomial transmission of these two strains on the intensive care units but no details of any further investigations were given.

PFGE of XbaI or SspI digests of chromosomal DNA was used to examine 64 clinical S. maltophilia isolates collected from 60 patients and the hands of one nurse over a 9-month period (419). Eight of the patients and the nurse were involved in an outbreak of S. maltophilia on an intensive care nursery. Although isolates from six of the eight patients had the same profile, the isolate from the hands of the nurse was unique. Turner-Hubbard et al. (416) used SpeI-based PFGE to demonstrate that isolates from bronchoalveolar lavage fluid were indistinguishable from those from bronchoscopes which had undergone defective sterilization procedures. More recently, Fabe et al. used this technique after XbaI or DraI digestion to examine strains from a hematology unit. They observed great genomic diversity among the strains analyzed but reported that person-to-person spread had occurred between several patients (117). An investigation into pulmonary colonization in cystic fibrosis patients by PFGE failed to demonstrate evidence of a common source of exposure or person-to-person spread among five patients (437).

RAPD, also known as arbitrarily primed PCR and multiple arbitrary amplicon profiling, has also been reported to be a useful tool for typing S. maltophilia. Its advantage over PFGE is that it is a more rapid and less labor-intensive method. However, there have been disagreements about which is the more discriminatory (420, 462).

RAPD as a single typing method has been used to type 130 S. maltophilia strains (51 from the hospital environment, 48 clinical, and 31 from other environments) collected over an 8-month period in a French hospital (84). Sixteen cases where pairs were indistinguishable by RAPD profiles were identified: nine clinical, five from the hospital environment, and two from soil. Some evidence of cross-infection between hematology and intensive care unit patients was identified, but there were no matches between environmental and clinical strains.

ERIC-PCR has also been used to successfully type S. maltophilia (67). A total of 38 clinical strains were examined, 9 from a burn unit, 20 epidemiologically unrelated isolates, and 9 from the same cystic fibrosis patient. The burn unit strains and the 20 other unrelated strains were independent. The nine strains collected from the sputum of the cystic fibrosis patient over a 22-month period were, however, indistinguishable. The authors compared ERIC-PCR with RAPD. Both yielded rapid, reproducible, and discriminatory fingerprints of S. maltophilia. However, the authors were of the opinion that interpretation of results was easier with ERIC-PCR.

Schable et al. used multilocus enzyme electrophoresis, in conjunction with serotyping, to investigate an outbreak of S. maltophilia infection on a shock-trauma intensive care unit (376). Although most of the outbreak strains belonged to serotype 10, strains of this serotype unrelated to the outbreak yielded different electrophoretic types on multilocus enzyme electrophoresis (376).

Despite the number of reported outbreaks in which there was identification of clusters of strains indistinguishable on typing (36, 369, 419, 433, 462), exact sources and modes of transmission of S. maltophilia have proved difficult to elucidate. The great diversity of strains identified within given institutions (84, 147), the relative frequency of isolation from a wide variety of environmental sites, and the culture from some of these sites of strains indistinguishable from associated clinical strains (405) suggest that multiple independent acquisitions from environmental sources could be an important mode of transmission of S. maltophilia.

CLINICAL MANIFESTATIONS OF S. MALTOPHILIA INFECTION

S. maltophilia is associated with an ever-expanding spectrum of clinical syndromes. However, many early publications failed to cite unequivocal evidence for infection with this organism. Indeed, the isolation of the bacterium in mixed culture, coupled with difficulties in distinguishing between colonization and true infection at superficial sites (such as skin ulcers or the upper respiratory tract) and the recovery of the bacterium as a contaminant of necropsy specimens (330), fostered the opinion expressed in earlier reports (145, 330, 390, 401) that S. maltophilia was an organism with strictly limited pathogenic potential which was rarely capable of causing disease in individuals other than those who were severely debilitated or immunocompromised. Holmes et al. considered that only 6 of 128 isolates submitted to a reference laboratory were associated with genuine infection (180). A more recent publication of a series of 68 patients from whom S. maltophilia was isolated concluded that only 9 patients had clinical evidence of infection with this organism (187). However, more recent studies that used stringent criteria for defining infection, coupled with isolation of the bacterium from normally sterile sites, have established beyond doubt that S. maltophilia can behave as a true pathogen. Although S. maltophilia is regarded as being primarily a nosocomial pathogen (33, 118, 262, 392), community-acquired infection with this bacterium may occur more frequently than was previously recognized (109, 172, 265). For example, Laing et al., in their series of 63 patients presenting to three acute-care hospitals, reported that 15 (23.8%) cases of infection and/or colonization with S. maltophilia were community acquired (241). In another study, 26 (24%) of 109 isolates were deemed to have been acquired in the community (462), and Southern and Schneider noted that 50% of strains in their series of 32 patients were isolated at the time of admission or from outpatients (390). Of the seven reported cases of S. maltophilia meningitis, only three were nosocomial in origin (295).

Bacteremia

Bacteremia is a common manifestation of S. maltophilia infection (116, 134, 197, 220, 222, 238, 241, 279, 284, 285, 301, 432) and appears to be increasing in frequency (238). Bacteremia may be secondary to a pulmonary, urinary, or gastrointestinal source (8, 388, 467, 470) although it is often not possible to determine the portal of entry. The importance of intravascular devices in the pathogenesis of S. maltophilia bacteremia is, however, becoming increasingly recognized (10, 28, 78, 115, 116, 138, 279, 284, 432), and in cases where there is no obvious source of infection it has been suggested that these devices may be the primary source. For example, Muder et al. report that in their series of 91 patients with S. maltophilia bacteremia, 56% did not have a clinically apparent portal of entry but 84% of these individuals had a central venous catheter in place (284). In several instances, it has been possible to identify environmental reservoirs from which S. maltophilia was likely to have been acquired. Flaherty et al. (130) investigated an outbreak of gram-negative bacteremia, including three cases caused by S. maltophilia and an additional case from which both S. maltophilia and Enterobacter cloacae were isolated from blood cultures. The source was identified as contaminated O-rings in reprocessed hemodialyzers. High-level O-ring contamination during simulated dialysis was demonstrated by Bland et al. to produce blood compartment contamination with S. maltophilia (40). Inadequate disinfection during reprocessing of capillary dialyzers was also implicated in another outbreak of S. maltophilia bacteremia (422). A cluster of cases reported by Fisher et al. (129) traced the source to contaminated pressure monitoring systems during open-heart surgery.

It is important to distinguish true S. maltophilia bacteremia from pseudobacteremia (197) arising from contamination of blood cultures when samples used to fill tubes for coagulation studies (which contain nonsterile anticoagulants such as sodium citrate) are then used to inoculate blood culture bottles (8, 378). This may be a more frequent occurrence than is generally recognized (8).

Relapsing S. maltophilia bacteremia has been described (36, 115, 285). Molecular typing techniques demonstrated that blood culture isolates from a patient who had experienced three episodes of bacteremia were indistinguishable.

Case/fatality ratios associated with S. maltophilia bacteremia may be high (36, 115, 285). In a series of 32 cases, Jang et al. noted that 22 (69%) were associated with a fatal outcome; 13 (41%) of these were deemed to be directly attributable to septicemia (197). Some investigators have also reported that polymicrobial bacteremia with S. maltophilia is a frequent occurrence (115). In their study, Jang et al. (197) noted that 44% of 32 cases of bacteremia were polymicrobial in origin. According to some investigators, the acute mortality rate associated with these polymicrobial bacteremias is not significantly different from that associated with bacteremia due to S. maltophilia alone (115, 197), although this is in contrast to the reports of others (238). S. maltophilia septicemia may be complicated by disseminated intravascular coagulation and purpura fulminans (208, 267). Ecthyma gangrenosum is also a well-recognized complication (52) (see the section on skin and soft tissue infection, below).

Endocarditis

There have been several reports of S. maltophilia endocarditis (15, 100, 115, 128, 168, 180, 197, 285, 378, 389, 399, 456, 464, 467, 470). Most of the cases have occurred in intravenous drug abusers or as a complication of prosthetic valve surgery. In the latter, infection often arises early in the postoperative period, possibly due to contaminated vascular access devices (115), although late-onset infections have been described (100, 115). Semel et al. reported a patient being treated for streptococcal prosthetic valve endocarditis who developed S. maltophilia superinfection, which they attributed to reflux of contaminated anticoagulant from collection tubes into the patient’s venous system (378). Endocarditis in the absence of drug abuse or cardiac valve abnormalities is uncommon (115, 389). For example, Gutierrez Rodero et al. described a case of endocarditis following infection of a ventriculoatrial cerebrospinal fluid (CSF) shunt in a patient with otherwise normal native cardiac valves (168). The prognosis of S. maltophilia endocarditis is variable. Although favorable outcomes with antimicrobial therapy alone have been recorded (168), surgical intervention to replace the infected valve may be necessary (467). The infection may be complicated by valve ring or myocardial abscesses and septic emboli (197, 285, 467).

A variety of other cardiovascular manifestations of S. maltophilia infection have been reported, including pericarditis (115, 470), infection of the pseudopericardial sac in an artificial heart recipient (101), and bacteremia in association with mitral valve prolapse (289).

Respiratory Tract Infection

S. maltophilia has been reported to account for 5% of nosocomial pneumonias (3), although several large studies of the etiology of nosocomial pneumonia have failed to find any cases associated with this bacterium (77, 351, 411). Nosocomial pneumonia has been observed during outbreaks of S. maltophilia infection, with several cases occurring over relatively short periods (220, 241, 308, 433).

The respiratory tract is the most common site of isolation of S. maltophilia in hospitalized patients, accounting for the origin of 56 to 69% of isolates (84, 147, 241, 279), although the majority of patients (53 to 71%) with S. maltophilia-positive respiratory tract cultures are colonized rather than infected at this site (220, 241, 433). More rigorous diagnostic criteria are necessary, therefore, if the distinction between colonization and true infection is to be made (137).

S. maltophilia nosocomial pneumonia is associated with mechanical ventilation, tracheostomy, previous exposure to broad-spectrum antibiotics, the use of respiratory tract equipment such as nebulizers (116, 220, 233, 241, 279, 308, 433, 470), and therapy with aerosolized polymyxin (122). Many patients also have preexisting lung conditions such as chronic obstructive pulmonary disease, bronchiectasis, kyphoscoliosis, or endobronchial obstruction (241, 247, 470). Pulmonary infection following lung transplantation has also been reported (465).

Respiratory tract involvement with S. maltophilia is associated with significantly increased mortality (279). Kollef et al. (233) reported that the isolation of a “high-risk” pathogen such as S. maltophilia was the most important predictor of mortality in late-onset ventilator-associated pneumonia. The mortality rate in neutropenic patients with pneumonia is 40% (220).

The source of S. maltophilia in these patients is often unclear (172). Although ventilator circuits have yielded the organism when sampled (255, 308, 433) this may have represented contamination from the patient rather than the source itself. Klick and Du Moulin (230) reported a cluster of cases on an intensive care unit in which an oxygen analyzer contaminated with S. maltophilia was implicated, and Korn et al. also described an outbreak associated with reusable in-line ventilator temperature probes (236). In their study, Turner-Hubbard et al. attributed the isolation of S. maltophilia from bronchoalveolar specimens to faulty bronchoscope sterilization protocols (416). Interestingly, they did not observe clinically overt infection as a result of using contaminated bronchoscopes.

Although several extensive studies of the etiology of community-acquired pneumonia have failed to identify a single case in which S. maltophilia was the cause (22, 54, 119, 120, 206, 261), a few cases of community-acquired pneumonia have been described (372); these mostly occurred in patients with predisposing conditions such as rheumatic heart disease and bronchiectasis (194, 388). The case reported by Irifune et al. is noteworthy because the isolate exhibited a mucoid phenotype (194). Gardner et al. (145) reported a case of S. maltophilia bacteremia secondary to aspiration pneumonia.

The first reported isolation of S. maltophilia from the respiratory tracts of patients with cystic fibrosis was in 1975 in Denmark by Frederiksen et al. (133). The prevalence of S. maltophilia in this patient group has been increasing, but variation between centers is well recognized. The prevalence rose from <2% in 1975 to 19% in 1993 in Denmark (133) and from 0% in 1983 to 10% in 1990 in one British center (154). It is now 19% in another British center (93) and over 30% in one Spanish center (16). The prevalence has generally been lower in the United States, ranging from 1.8 to 8.7% (89, 283). The reasons for this increase are not clear, but one study suggested that the amount of antipseudomonal antibiotics with which these patients were treated and the duration of hospitalization were important risk factors (154). S. maltophilia may persist for long periods in the sputum of patients colonized with the bacterium (24). Recently, in a comparison of four different methods for preculture treatment of sputum samples from cystic fibrosis patients, Hoppe et al. found no significant effect on S. maltophilia isolation rates (181), although the use of selective media may affect the ability of clinical laboratories to demonstrate the presence of the bacterium in sputum (92).

There is no evidence to date of any nosocomial transmission of S. maltophilia to cystic fibrosis patients (94, 437).

The prognostic significance of S. maltophilia in the respiratory tract of cystic fibrosis patients is unclear. Some studies have shown no evidence of an adverse clinical outcome (89), whereas others have reported progressive deterioration in pulmonary function, particularly in patients chronically colonized for long periods with bacterial counts of S. maltophilia in excess of 105 to 106 CFU/ml of sputum (16, 207, 231). For a more detailed discussion of S. maltophilia in cystic fibrosis, the reader is referred to the recent review by Denton (91).

Instances of true infection of the upper respiratory tract appear very rare. The clinical significance of the isolation of S. maltophilia from pharyngeal swabs (185, 186, 401) is uncertain. Harlowe reported a single case of S. maltophilia acute mastoiditis in a patient who developed acute otitis media after swimming (170).

Central Nervous System Infection

Meningitis caused by S. maltophilia is uncommon (183). In neonates and infants, the infections appear spontaneous in onset (90, 373), whereas those in adults are secondary to neurosurgical procedures (153, 285, 295, 415). The presence of foreign material such as CSF shunts, ventriculostomy tubes, and Ommaya reservoirs may be important in the pathogenesis of these infections (295). Additionally, a spinal epidural catheter was deemed to have predisposed a patient to the development of a spinal epidural abscess (438). Adult cases of S. maltophilia meningitis in the absence of antecedent neurosurgery are very rare (327). The recently proposed species, S. africana, as described by Drancourt et al., was isolated from the CSF of a human immunodeficiency virus-seropositive Rwandan refugee with clinical signs of meningoencephalitis (104).

Ophthalmologic Infection

Ocular infections associated with S. maltophilia appear to be increasing in incidence (331). A variety of ophthalmologic syndromes have been reported, including conjunctivitis, keratitis, dacryocystitis, and preseptal cellulitis (28, 331, 373, 386, 390, 401). Conjunctivitis, keratitis, and corneal ulcers in contact lens wearers from whom the bacterium has been isolated have also been described (237, 331, 393). Chen et al. (68) reported a case of endophthalmitis following the implantation of a sustained-release preparation of ganciclovir. Endophthalmitis has also been described following cataract extraction (204). S. maltophilia has been isolated from contact lenses or lens care paraphernalia (73, 103, 211, 331), and it has been suggested that synergy between S. maltophilia and Acanthamoeba spp. may be important in the pathogenesis of contact lens-associated amebal keratitis (49, 50).

Urinary Tract Infection

Although S. maltophilia has been frequently isolated from urine specimens, early reports acknowledged that there was insufficient evidence to support an unequivocal role for this bacterium as a urinary tract pathogen (145, 150, 180, 287, 401). Therefore, it has come to be considered an uncommon cause of urinary tract infection (470). In most patients, the infection is acquired in the hospital setting (241) and is usually secondary to urinary tract surgery or instrumentation, including catheterization (148, 220, 470), or against a background of structural urinary tract abnormality (428). Wishart and Riley (455) reported an outbreak of nosocomial infection in which the source was identified as a contaminated disinfectant used for bladder instillation. Community-acquired infection appears rare (265).

Peritonitis in patients undergoing chronic ambulatory peritoneal dialysis has been observed (29, 324, 403, 404). This may follow Tenckhoff cannula exit-site infection, although most S. maltophilia exit-site infections do not appear to progress to peritonitis (83).

Urethritis, periurethral abscess, and epididymitis have also been reported (150, 180, 401). Garcia et al. described the isolation of the bacterium from semen specimens from fertile men (140).

Skin and Soft Tissue Infection

S. maltophilia is a relatively frequent isolate from wounds and other skin lesions (148, 150, 180, 220, 279, 390). However, a paucity of clinical details, coupled with incomplete information on microbiologic and other diagnostic criteria, often make it difficult to establish an unequivocal role for S. maltophilia as a pathogen in this context (250, 262, 330, 429), particularly when the organism is isolated in mixed culture. Improved diagnostic criteria may, in the future, allow the distinction between true infection and colonization (241).

Wound sepsis may follow accidental injury (148, 150, 330) including accidents in the workplace (4, 109, 155). Infection also occurs after surgical trauma (148, 150) and at sites where cutaneous defenses have been breached iatrogenically, such as tracheostomies and suprapubic (115), Tenckhoff, and vascular catheter sites (115, 429).

Primary and metastatic S. maltophilia cellulitis is reported increasingly from patients with solid-organ or hematologic malignancy. In a series of 114 cases of S. maltophilia infection in cancer patients, Vartivarian et al. reported 11 cases of cellulitis (429). Metastatic cellulitis may manifest as ecthyma gangrenosum. Although more commonly associated with P. aeruginosa bacteremia, this syndrome is a recognized feature in systemic S. maltophilia infection in oncology patients (52, 115, 197, 215, 285, 429). Recently, a syndrome of metastatic cellulitis associated with nodular skin lesions in individuals with leukemia has been described (429). These lesions may mimic disseminated fungal infections and are associated with a poor prognostic outcome. S. maltophilia is also associated with mucocutaneous and perineal lesions in patients with malignancy (287, 334, 429).

Other manifestations of S. maltophilia soft tissue infection include umbilical cellulitis (455), prepatellar bursitis (318), infections of burn wounds (210), cat scratches, and human bite wounds (390).

Bone and Joint Infection

Bone and joint infections are uncommon. They may follow orthopedic surgery (148, 150, 172) or trauma (17). Sequeira et al. reported a case of pubic symphysis infection in an intravenous drug abuser from whom S. maltophilia and P. aeruginosa were isolated (379).

Gastrointestinal Infection

Although asymptomatic fecal carriage of S. maltophilia has been noted in several reports (see the section on habitat, above), the bacterium appears to be an infrequent cause of gastrointestinal infection. Isolation from ascitic fluid and from intra-abdominal abscesses (including liver abscesses) has been recorded (102, 107, 286, 390), and five cases of cholangitis caused by S. maltophilia, all of which were secondary to biliary tract obstruction associated with malignancy, have also been described (317, 470). Zuravleff and Yu (470) cited a case of bacteremia subsequent to gastroenteritis, although it is unclear whether the two events were causally related. Minah et al. noted the appearance of S. maltophilia in the oral flora of cancer patients undergoing myelosuppressive chemotherapy, but they did not observe symptoms of acute infection in these individuals (272).

It has been suggested that cell wall defective variants of S. maltophilia may play a role in the pathogenesis of Crohn’s disease and ulcerative colitis (321, 322). Graham et al. used DNA hybridization techniques to identify sequences with homology to S. maltophilia in patients with chronic inflammatory bowel disease (CIBD) but concluded that the role of the bacterium in the natural history of CIBD has not been established unequivocally (158). Additional immunologic, serologic, and immunocytochemical evidence does not support its role in CIBD (190, 443, 444).

MANAGEMENT OF S. MALTOPHILIA INFECTION

In Vitro Susceptibility Testing

Infections caused by S. maltophilia are particularly difficult to manage because clinical isolates are frequently resistant to many antimicrobial agents (see below). These difficulties are compounded by methodological problems associated with susceptibility testing. Disk diffusion methods are deemed inaccurate and of poor reproducibility (178, 268, 315, 316, 462), with marked variations in results observed when zone diameters were measured after 24 and 48 h of incubation (315, 316). Quinolone agents, particularly ciprofloxacin, appear most problematic in this respect (20, 161, 316, 354), although Arpi et al. reported that disk diffusion was as reliable as Etest and agar dilution in determining the susceptibility of 124 clinical isolates of S. maltophilia to ciprofloxacin (11). In a study of 33 clinical isolates comparing agar dilution and disk diffusion tests, Hohl et al. (178) observed a 12% very major error rate and 58% minor error rate with ciprofloxacin. Although most workers have noted that erroneous disk diffusion tests overstate the activity of quinolones against S. maltophilia, false resistance has also been reported (161). The National Committee for Clinical Laboratory Standards currently recommends agar or broth dilution methods for S. maltophilia (290). These methods, however, are time-consuming, and alternative methods such as the Etest (AB Biodisk Solna Sweden) have been evaluated (316). Yao et al. compared the Etest with an agar dilution method by using 176 clinical isolates of S. maltophilia and reported an overall agreement of 94% between the two techniques (463), although Pankuch et al. noted that MICs of ticarcillin-clavulanate obtained with by technique did not correspond well to those obtained by four other methods (316).

A number of factors have been cited as affecting results of susceptibility testing. With respect to drugs of the β-lactam class, these include both the type (111) and nutrient concentration of susceptibility medium used (45). Hawkey et al. noted that the concentration of Zn2+ in the test medium influences the observed susceptibility of S. maltophilia to imipenem, although variations in Ca2+ and Mg2+ concentration had no such effect (171). A similar phenomenon was not observed for the Zn2+ concentration and meropenem (75). This observed effect does not appear to be mediated by a direct effect of the zinc ions on the zinc-dependent L1 β-lactamase (see below) of S. maltophilia (46). Divalent cation concentrations have, however, been reported to affect the MICs of the carboxy- and ureidopenicillins (82, 124). Similar effects have been observed with tetracycline, polymyxin B, aminoglycosides, and trimethoprim-sulfamethoxazole (82, 124).

Tilton et al. observed differences in the MICs of gentamicin and tobramycin in a comparison of broth and agar techniques (408). The incubation temperature also influences the results obtained on susceptibility testing, with aminoglycosides and polymyxin B appearing less susceptible when the bacteria are incubated at 30°C (320, 365, 442).

Resistance of Antimicrobial Agents

S. maltophilia is resistant to many currently available broad-spectrum antimicrobial agents. Particularly noteworthy is the resistance to drugs of the β-lactam class. Initially, resistance to these agents was thought to be conferred by two enzymes designated L1 and L2 (370, 371). The former, produced by virtually all wild-type strains (329), belongs to the metalloenzyme family, although the deduced amino acid sequence shows significant differences from that of other enzymes of this class such as the β-lactamases produced by Aeromonas hydrophila and Bacillus cereus (126, 439). These enzymes are dependent on the presence of Zn2+ at the active site. Although the zinc moiety in L1 can be replaced by Co2+, Cd2+, or Ni2+, these enzymes are less active than the native enzyme (35). The holoenzyme, which consists of a tetramer of four equal subunits, hydrolyzes a broad range of drugs of the β-lactam class, albeit with different degrees of catalytic efficiency (125). It exhibits predominantly penicillinase activity, although it is unable to hydrolyze aztreonam. It has been the subject of much attention, however, because of its ability to hydrolyze carbapenems such as imipenem and meropenem. It is not susceptible to β-lactamase inhibitors, such as clavulanate, although Payne et al. have very recently reported the inhibition of L1, and other metallo-β-lactamases by mercaptoacetic acid thiol ester derivatives (328). Following experiments with a purified enzyme from Bacillus cereus, they proposed that hydrolysis of these compounds by metallo-β-lactamases yields mercaptoacetic acid, which forms a disulfide link with a cysteine residue at the active site (328). In contrast to L1, L2, which exists as a dimer in its native state, is an enzyme with a serine active site. Comparison of the amino acid sequence of L2 with other enzymes has shown that it is most closely related to the TEM β-lactamase (440). It exhibits principally cephalosporinase activity but also hydrolyzes aztreonam (370). Unlike L1, this enzyme is susceptible to β-lactamase inhibitors. Although L2 is more susceptible to clavulanate than to tazobactam or sulbactam, there appears to be no correlation between the susceptibility to a β-lactamase inhibitor and the MIC of a β-lactam–inhibitor combination (341). Both L1 and L2 are chromosomally encoded and are inducible, and there is evidence that they share regulatory components (5, 364). Bonfiglio et al., however, recently described a clinical isolate of S. maltophilia with low-level expression of the L1 β-lactamase which retained inducibility for the L2 enzyme (47). In addition, Payne et al. (329) reported another clinical isolate of the bacterium which elaborated high levels of carbapenemase without induction and suggested that this strain might have a mutation in its regulatory gene(s) which allowed the constitutive production of significant levels of enzyme.

The existence of additional β-lactamases produced by S. maltophilia was first suggested by Cullman and Dick (80), who described the presence of six distinct enzymes in 20 clinical strains of the bacterium. Subsequent reports have confirmed the heterogeneity of β-lactamase production in S. maltophilia, with the additional enzymes categorized as either serine enzymes or metalloenzymes (80, 326). Poor diffusion of penicillins and cephalosporins across the bacterial cell membrane has also been suggested as contributing to resistance to these compounds (79, 269), although it is unclear whether this arises from quantitative or qualitative differences in porin channels (79, 459). More recently, there have been instances of transferable cephalosporin and aztreonam resistance from nosocomial strains of S. maltophilia to recipient strains of E. coli, Proteus mirabilis, and P. aeruginosa (14, 188). Kelly et al. reported transferable penicillin and cefazolin resistance in a clinical strain of S. maltophilia associated with a 5.6-kb plasmid (212). There have been no recorded instances of transferable carbapenem resistance.

Resistance to aminoglycosides mediated by aminoglycoside-modifying enzymes is apparently uncommon in S. maltophilia (335). King et al. (225) described the production of aminoglycoside 6′-N-acetyltransferase by a single isolate of the bacterium. Vanhoof et al. (423), in their study of six clinical isolates, reported the expression of an aminoglycoside-O-nucleotidyltransferase and aminoglycoside 6′-N-acetyltransferase in one strain. Reduced uptake of aminoglycosides is possibly the most important mechanism which determines resistance to these compounds. Temperature-dependent aminoglycoside resistance was initially attributed to changes in outer membrane profiles (446).

More recent evidence from strains exhibiting both temperature-dependent and -independent resistance suggests that an altered cell surface microenvironment secondary to changes in the O side chains of lipopolysaccharides (347, 348, 423) is a more likely mechanism, with changes of the phosphate content of lipopolysaccharide at lower growth temperatures correlating well with decreased aminoglycoside susceptibility (349). Yu et al. reported the emergence of amikacin resistance in an isolate from a patient with infective endocarditis (467). Resistance was transferable to a strain of P. aeruginosa, but the mechanism of resistance was not investigated.

Resistance to quinolone agents is less well characterized. Resistant mutants are readily selected in vitro and are associated with qualitative and quantitative changes in outer membrane proteins (246). Cross-resistance to chloramphenicol and doxycycline in quinolone-resistant isolates has been reported by Lesco-Bornet et al. (246). The development of antimicrobial resistance in vivo has received comparatively little attention (69, 294). Manian et al. noted that 50% of 10 isolates lost susceptibility to at least one antibiotic during repeated isolations from intensive care unit patients (256). However, serial isolates were not subjected to a pheno- or genotypic typing technique, and the possibility of exogenous acquisition of a more resistant strain cannot be excluded. However, Garrison et al. used PFGE to demonstrate that resistant strains of S. maltophilia recovered from patients following therapy were indistinguishable from pretreatment isolates. In addition, they developed an in vitro pharmacodynamic chamber model, which permitted the observation of emergence of multiple resistance phenotypes during exposure to ceftazidime, ciprofloxacin, gentamicin, and ticarcillin-clavulanate (146).

Recently, Alonso and Martinez reported the presence of at least one multidrug resistance system in S. maltophilia, selected for by exposure to low concentrations of tetracycline. This energy-dependent efflux mechanism is effective against quinolones and chloramphenicol, as well as tetracyclines, but not against aminoglycosides or β-lactam drugs (6).

Selection of Antimicrobial Agents

The selection of agents for use in the management of S. maltophilia infection presents a challenge to laboratarians and clinicians alike, not merely because of the aforementioned problems associated with susceptibility testing and the inherent resistance of the bacterium to many agents. While there is no shortage of in vitro studies of the activity of antimicrobial agents against S. maltophilia, there is a paucity of clinical investigations to determine the optimal therapy of infections associated with the bacterium; in particular, there have been no controlled trials, and recommendations for therapy are often based on retrospective studies and anecdotal reports.

Table Table66 shows the susceptibility of S. maltophilia strains to selected antimicrobial agents. The wide range of values is, at least in part, explicable by differences in the susceptibility testing methods used by the investigators which, as noted above, may significantly influence the observed results. Differing criteria for the definition of susceptibility and resistance and also the fact that some investigators have tested limited numbers of isolates also compound the difficulties in comparing studies.

TABLE 6
Susceptibility of S. maltophilia to selected antimicrobial agents

There have also been very few studies which have examined the antimicrobial susceptibility of strains from disparate locations. Sader et al. tested isolates from the United States, Brazil, and Switzerland, although their results do not give a detailed comparison between country of origin and antimicrobial susceptibility (369). Despite their limitations, it is possible to draw general conclusions from the available data and to make broad recommendations for the therapy of S. maltophilia infection. With few exceptions (142, 427) most studies have found trimethoprim-sulfamethoxazole to be active against most strains of the bacterium, and this drug has long been regarded as the agent of choice for the therapy of S. maltophilia infection (113, 118, 178, 276, 355). This is despite the view that this drug is only bacteriostatic for most isolates, a fact which has prompted some authorities to recommend that this compound be used at close to the maximum tolerated doses (427). Toxicity of the sulfonamide component of the combination may prove to be a limitation of this approach (113). Resistance to trimethoprim-sulfamethoxazole has long been recognized (276). Although resistance to this drug may be increasing, Vartivarian et al. noted an increase in the trimethoprim-sulfamethoxazole susceptibility of isolates at the M. D. Anderson Cancer Center over a 12-year period. They attributed this to the discontinuation of this drug as a commonly used agent of antibacterial prophylaxis. Not unexpectedly, they observed a parallel increase in resistance to the quinolones—the compounds which replaced trimethoprim-sulfamethoxazole in this role—over the same period (427). Recently, Muder et al. suggested that a combination of trimethoprim-sulfamethoxazole and either ticarcillin-clavulanate or an extended-spectrum cephalosporin may be superior to trimethoprim-sulfamethoxazole alone (284).

There is near-universal agreement that the penicillins and cephalosporins, with a few exceptions, exhibit poor activity against S. maltophilia. The resistance of the bacterium to carbapenems, including newer members of this class (406) such as biapenem (367), is well recognized, although variations in the activity of these compounds have been noted. Piddock and Turner reported that three strains of S. maltophilia which were resistant to imipenem were susceptible to meropenem (336). Although several studies have shown that most strains tested are susceptible to the oxa-β-lactam moxalactam (Table (Table6)6) (397), the hematologic side effects of this agent have precluded its continuing use in clinical practice. Of the extended-spectrum cephalosporins, ceftazidime appears to possess reasonable activity (144), although it must be stated that this is highly variable between strains, and this compound cannot be recommended for use as empirical therapy. Ticarcillin-clavulanate has been noted by several investigators to exhibit good activity against S. maltophilia, and it has been suggested that this agent should be used as the agent of choice in individuals intolerant of trimethoprim-sulfamethoxazole. In contrast, other β-lactam–β-lactamase inhibitor combinations such as piperacillin-tazobactam (58, 122, 391), amoxicillin-clavulanate, and ampicillin-sulbactam (142) are poorly active against the bacterium. Only Fujita et al. have reported that 8 of 10 strains isolated from patients with S. maltophilia pneumonia were susceptible to a combination of cefoperazone and sulbactam (137).

Similarly, other combinations which have been evaluated, such as aztreonam-sulbactam, aztreonam-tazobactam (142), and clavulanic acid combined with carbenicillin, imipenem, ceftazidime, or aztreonam (142, 143), do not offer increased activity against the bacterium with the exceptions of 2:1 and 1:1 (wt/wt) aztreonam-clavulanic acid (11, 143). However, the differing pharmacokinetics of these two agents dictate that levels of clavulanic acid in plasma decrease more rapidly than those of aztreonam, and the clinical applicability of this combination may be limited (143, 427). Rouse et al. reported synergy with a combination of cefoperazone and sulbactam in the treatment of S. maltophilia experimental pneumonia in mice (366), and Elkhaili et al. observed increased in vitro activity of a cefepime-clavulanic acid combination compared to the activities of the agents when used singly (113). It is unlikely that agents of the trinem (formerly tribactam) class of β-lactams will have any useful role in the management of S. maltophilia infection (454).

Susceptibility to early examples of the quinolone class of antimicrobial agents, including ciprofloxacin (Table (Table6),6), varies markedly, but there have been anecdotal reports of response to these agents in systemic S. maltophilia infection (294, 457). However, both superinfection by S. maltophilia in patients receiving quinolones and therapeutic failures of S. maltophilia infection have been documented (69, 294), and the use of these compounds as empirical therapy must be considered with care. Newer quinolones, such as clinafloxacin, sparfloxacin, and trovafloxacin, appear to be more active against the bacterium than do the older agents in this class (23, 34, 62, 71, 88, 121, 131, 136, 182, 199, 221, 223, 224, 241, 251, 259, 315, 344346, 350, 359361, 368, 369, 391, 427). Pankuch et al., for example, reported that 93% of 25 ciprofloxacin-resistant strains were susceptible to clinafloxacin (315). Although these in vitro studies appear promising, there are at present few data on the use of the newer quinolones in the clinical setting, and the results of clinical studies are awaited with interest.

The activity of the aminoglycosides, including newer members of this class such as isepamicin (198, 221), against S. maltophilia is disappointing, and these agents, in general, play a very limited role as monotherapy. In vitro synergy has been observed when these agents have been used in combination with other antimicrobial agents (see below). The observation that liposomal preparations of some aminoglycosides are associated with decreased MICs compared with those of the free compound deserves further investigation (307).

Minocycline and doxycycline exhibit good in vitro activity against S. maltophilia, in marked contrast to tetracycline itself (Table (Table6)6) (300, 408), although clinical experience with these agents is extremely limited. Chloramphenicol has also been reported by several investigators (Table (Table6)6) as having good activity against the bacterium, and there are anecdotal reports of therapeutic success with this drug (20). The potential for hematologic side effects is of particular importance, and since many patients at risk of S. maltophilia infection have underlying disease-related or iatrogenic myelosuppression, chloramphenicol is not widely used in clinical practice. Because of the disappointing outcomes achieved with monotherapy in the management of S. maltophilia infection, it is not surprising that several investigators have proposed the use of combinations of antimicrobial agents, with much effort focusing on the identification of those two- or three-drug combinations which demonstrate in vitro synergy against the bacterium (30, 66, 72, 124, 156, 286, 299, 340, 362, 466).

It is difficult to draw firm conclusions from these studies, not only because of strain-to-strain variation and the wide variety of combinations tested but also because of the differing methods used. These include broth and agar dilution, checkerboard, and half-checkerboard techniques, as well as time-kill curves. Indeed, variations within studies have been observed in which combinations identified to be synergistic by the checkerboard method were found not to be so by killing-curve criteria (66, 124, 340). In addition, synergy may be strain dependent (88, 156). Furthermore, although combinations with demonstrable synergy in the laboratory setting have been associated with successful therapeutic outcomes, other combinations deemed to be nonsynergistic in vitro have also been associated with favorable clinical results (467). Moreover, it is important to note that although synergy between combinations of drugs may be demonstrable, synergy may not occur at clinically achievable concentrations (72). For example, in their investigation of the use of aerosolized amiloride in the therapy of Pseudomonas infections in cystic fibrosis patients, Cohn et al. were able to demonstrate synergy between amiloride and tobramycin against three strains of S. maltophilia (74). However, this phenomenon was observed only at levels of amiloride in excess of those achievable in clinical practice. Studies in which synergy was demonstrated are summarized in Table Table7.7.

TABLE 7
Combinations of antimicrobial agents showing in vitro synergy against S. maltophilia

Few data on the use of combinations of antimicrobial agents in clinical practice have been published, and they are derived from anecdotal evidence (168, 467) and noncontrolled studies (284), but the utility of these therapeutic approaches clearly deserves further study.

Management of Infection by Means Other than Antimicrobial Agents

In addition to antimicrobial chemotherapy in the management of S. maltophilia infection, several investigators have stressed the importance of removing infected vascular access devices (27, 115, 429) or prosthetic material (327, 415). Muder et al., however, reported the successful management of central venous catheter-related bacteremia without removal of the device (284).

Prognosis

Several investigators have examined factors which influence the outcome in S. maltophilia infection. In their prospective multicenter study of 91 cases of bacteremia, Muder et al. (284) found that hematologic malignancy, transplantation, neutropenia, immunosuppressive therapy, and a high severity of illness score (based on temperature, presence of hypotension, mental status, and the need for ventilatory support) were important. In contrast to other investigators (238), Muder et al. did not find a significant difference in acute mortality if S. maltophilia bacteremia was polymicrobial or monomicrobial in origin. They were unable to demonstrate a significant association between survival and administration of appropriate antimicrobial therapy (unlike another study [220]), although they acknowledged that the number of patients classified as being inappropriately treated may have been too small to allow meaningful statistical analysis.

PREVENTION OF S. MALTOPHILIA INFECTION

Several strategies to prevent S. maltophilia infection have been proposed. These include avoidance of inappropriate antibiotic use and of prolonged implantation of foreign devices (118). Maintenance and, where appropriate, disinfection and/or sterilization of respiratory therapy equipment, cardiopulmonary bypass apparatus, hemodialyzers, and ice-making machines are also important (61, 129, 130, 274, 308, 342, 422, 433, 455). In addition, it may be prudent for neutropenic patients to avoid drinking noncarbonated bottled water, although carbonated water is acceptable (219).

During nosocomial epidemics of S. maltophilia colonization and/or infection, reinforcement of hand hygiene practices and wearing of gloves when handling contaminated respiratory secretions and wound drainage are of benefit (38, 172, 433). The cost-effectiveness of screening programs for S. maltophilia colonization in high-risk patients (175) requires further investigation before they can be recommended.

CONCLUDING REMARKS

Despite the recognition of S. maltophilia as a significant human pathogen, primarily in the nosocomial but also in the community setting, comparatively little is known about the bacterium, particularly with regard to putative virulence factors. With continuing advances in medical technology, including treatment regimens which are associated with iatrogenic immunosuppression, and the growth of at-risk populations, such as those with AIDS, the incidence of infection associated with S. maltophilia will almost certainly increase. Management of these infections presents problems for both the laboratorian and clinician. In particular, methods for determining the susceptibility of S. maltophilia to antimicrobial agents, which are at present often unreliable, require further development. The role of alternative therapeutic agents in the management of S. maltophilia infection, particularly the newer quinolones, deserves continued examination. Similarly, there is a need to evaluate in the clinical setting the utility of antimicrobial combinations which have been shown to exhibit in vitro synergy against the bacterium. Much remains to be understood of the epidemiology of S. maltophilia, although the development of rapid, inexpensive, and reproducible typing systems, coupled with the availability of selective culture media, will permit systematic investigation of this topic. In particular, more information on nosocomial reservoirs and routes of transmission of the bacterium is needed; this is essential for the development of effective infection control strategies. It is likely, however, that S. maltophilia will present a major challenge to microbiologists, clinicians, and hospital epidemiologists for some time to come.

ACKNOWLEDGMENT

We thank Andleeb Qureshi for assistance in preparation of the manuscript.

REFERENCES

1. Abussaud M, Mahawreh B. Pseudomonas flora of citrus—plant nurseries in the Jordan valley. Pak J Bot. 1994;26:235–240.
2. Acevedo H F, Slifkin M, Pouchet G R, Pardo M. Immunohistological localisation of a chorio-gonadotrophin-like protein in bacteria isolated from cancer patients. Cancer. 1978;41:1217–1222. [PubMed]
3. A’Court G, Garrard C S. Nosocomial pneumonia in the intensive care unit: mechanisms and significance. Thorax. 1992;47:465–473. [PMC free article] [PubMed]
4. Agger W A, Cogbill T H, Busch H, Jr, Landercasper J, Callister S M. Wounds caused by corn-harvesting machines: an unusual source of infection due to gram-negative bacilli. Rev Infect Dis. 1986;8:927–931. [PubMed]
5. Akova M, Bonfiglio G, Livermore D M. Susceptibility to beta-lactam antibiotics of mutant strains of Xanthomonas maltophilia with high- and low-level constitutive expression of L1 and L2 beta-lactamases. J Med Microbiol. 1991;35:208–213. [PubMed]
6. Alonso A, Martinez J L. Multiple antibiotic resistance in Stenotrophomonas maltophilia. Antimicrob Agents Chemother. 1997;41:1140–1142. [PMC free article] [PubMed]
7. Anonymous. Pseudomonas in hatching eggs. Can Poult Rev. 1974;49:18. , 20, 22.
8. Aoun M, Van der Auwera P, Devleeshouwer C, Daneau D, Seraj N, Meunier F, Gerain J. Bacteraemia caused by non-aeruginosa Pseudomonas species in a cancer centre. J Hosp Infect. 1992;22:307–316. [PubMed]
9. Arella M, Sylvestre M. Production of an extracellular ribonuclease by Pseudomonas maltophilia. Can J Microbiol. 1979;25:321–328. [PubMed]
10. Arpi M, Victor M A, Moller J K, Jonsson V, Hansen M M, Peterslund N A, Bruun B. Changing etiology of bacteremia in patients with hematological malignancies in Denmark. Scand J Infect Dis. 1994;26:157–162. [PubMed]
11. Arpi M, Victor M A, Mortensen I, Gottschau A, Bruun B. In vitro susceptibility of 124 Xanthomonas maltophilia (Stenotrophomonas maltophilia) isolates: comparison of the agar dilution method with the E-test and two agar diffusion methods. APMIS. 1996;104:108–114. [PubMed]
12. Aucken H M, Pitt T L. Lipopolysaccharide profile typing as a technique for comparative typing of gram-negative bacteria. J Clin Microbiol. 1993;31:1286–1289. [PMC free article] [PubMed]
13. Aznar R, Alcaide E, Garay E. Numerical taxonomy of pseudomonads isolated from water sediment and eels. Syst Appl Microbiol. 1992;14:235–246.
14. Babalova M, Blahova J, Lesicka-Hupkova M, Krcmery V, Kubonova K. Transfer of ceftazidime and aztreonam resistance from nosocomial strains of Xanthomonas (Stenotrophomonas) maltophilia to a recipient strain of Pseudomonas aeruginosa ML-1008. Eur J Clin Microbiol Infect Dis. 1995;14:925–927. [PubMed]
15. Baddour L M, Meyer J, Henry B. Polymicrobial infective endocarditis in the 1980s. Rev Infect Dis. 1991;13:963–970. [PubMed]
16. Ballestero S, Virseda I, Escobar H, Suarez L, Baquero F. Stenotrophomonas maltophilia in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis. 1995;14:728–729. [PubMed]
17. Baltimore R S, Jenson H B. Puncture wound osteochondritis of the foot caused by Pseudomonas maltophilia. Pediatr Infect Dis J. 1990;9:143–144. [PubMed]
18. Bandin I, Heinen P, Brown L L, Toranzo A E. Comparison of different ELISA kits for detecting Renibacterium salmoninarum. Bull Eur Assoc Fish Pathol. 1996;16:19–22.
19. Barry A L, Badal R E. Reliability of early identifications obtained with Enterobacteriaceae-Plus biochemical cards in the AutoMicrobic system. J Clin Microbiol. 1982;16:257–265. [PMC free article] [PubMed]
20. Barry A L, Fass R J, Anhalt J P, Neu H C, Thornsberry C, Tilton R C, Painter B G, Washington J A., II Ciprofloxacin disk susceptibility tests: interpretive zone size standards for 5-microgram disks. J Clin Microbiol. 1985;21:880–883. [PMC free article] [PubMed]
21. Baruchel, A., O. Hartmann, A. Andremont, and C. Tancrede. 1986. Severe gram-negative infections in neutropenic children cured by imipenem/cilastatin in combination with an aminoglycoside. J. Antimicrob. Chemother. 18(Suppl. E):167–173. [PubMed]
22. Bates J H, Campbell G D, Barron A L, McCracken G A, Morgan P N, Moses E B, Davis C M. Microbial etiology of acute pneumonia in hospitalised patients. Chest. 1992;100:1005–1012. [PubMed]
23. Bauernfeind A. Comparative in-vitro activities of the new quinolone, Bay y 3118, and ciprofloxacin, sparfloxacin, tosufloxacin, CI 960 and CI 990. J Antimicrob Chemother. 1993;31:505–522. [PubMed]
24. Bauernfeind A, Bertele R M, Harms K, Horl G, Jungwirth R, Petermuller C, Przyklenk B, Weisslein-Pfister C. Qualitative and quantitative microbiological analysis of sputa of 102 patients with cystic fibrosis. Infection. 1987;15:270–277. [PubMed]
25. Belcour B, Courtois D, Ehret C, Petiard V. Rapid production of irones by maturation of orris rhizomes by two bacterial strains. Phytopathology. 1993;34:1313–1315.
26. Bell E B. An immune-type agglutination of mouse spermatozoa by Pseudomonas maltophilia. J Reprod Fertil. 1968;17:275–283. [PubMed]
27. Benezra D, Kiehn T E, Gold J W M, Brown A E, Turnbull A D M, Armstrong D. Prospective study of infections in indwelling central venous catheters using quantitative blood cultures. Am J Med. 1988;85:495–498. [PubMed]
28. Ben Tovim T, Eylan E, Romano A, Stein R. Gram-negative bacilli isolated from external eye infections. Infection. 1974;2:162–165. [PubMed]
29. Berbari N, Johnson D H, Cunha B A. Xanthomonas maltophilia peritonitis in a patient undergoing peritoneal dialysis. Heart Lung. 1993;22:282–283. [PubMed]
30. Berenbaum M C, Yu V L, Felegie T P. Synergy with double and triple antibiotic combinations compared. J Antimicrob Chemother. 1983;12:555–563. [PubMed]
31. Berg G, Balling G. Bacterial antagonists to Verticillium dahliae. J Phytopathol. 1994;141:99–110.
32. Berg G, Marten P, Balling G. Stenotrophomonas maltophilia in the rhizosphere of oil-seed rape—occurrence, characterisation, and interaction with phytopathogenic fungi. Microbiol Res. 1996;151:19–27.
33. Bergogne-Berezin, E., D. Decre, and M. L. Joly-Guillou. 1993. Opportunistic nosocomial multiply-resistant bacterial infections—their treatment and prevention. J. Antimicrob. Chemother. 32(Suppl. A):39–47. [PubMed]
34. Biedenbach D J, Sutton L D, Jones R N. Antimicrobial activity of CS-940, a new trifluorinated quinolone. Antimicrob Agents Chemother. 1995;39:2325–2330. [PMC free article] [PubMed]
35. Bicknell R, Emanuel E L, Gagnon J, Waley S G. The production and molecular properties of the zinc beta-lactamase of Pseudomonas maltophilia IID 1275. Biochem J. 1985;229:791–797. [PMC free article] [PubMed]
36. Bingen E H, Denamur E, Lambert-Zechovsky N Y, Bourdois A, Mariani-Kurkdjian P, Cezard J-P, Navarro J, Elion J. DNA restriction fragment length polymorphism differentiates crossed from independent infections in nosocomial Xanthomonas maltophilia bacteremia. J Clin Microbiol. 1991;29:1348–1350. [PMC free article] [PubMed]
37. Binks P R, Nicklin S, Bruce N C. Degradation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) by Stenotrophomonas maltophilia PB1. Appl Environ Microbiol. 1995;61:1318–1322. [PMC free article] [PubMed]
38. Bjerke H S, Leyerle B, Shabot M M. Impact of ICU infections on outcome from surgical care. Am Surg. 1991;57:798–802. [PubMed]
39. Blake R C, Choate D M, Bardhan S, Revis N, Barton L L, Zocco T G. Chemical transformation of toxic metals by a Pseudomonas strain from a toxic waste site. Environ Toxicol Chem. 1993;12:1365–1376.
40. Bland L A, Arduino M J, Aguero S M, Favero H S. Recovery of bacteria from reprocessed high flux dialyzers after bacterial contamination of the header spacers and O rings. ASAIO Trans. 1989;35:314–316. [PubMed]
41. Blazevic D J. Current taxonomy and identification of non-fermentative gram-negative bacilli. Hum Pathol. 1976;7:265–275. [PubMed]
42. Boethling R S. Purification and properties of a serine protease from Pseudomonas maltophilia. J Bacteriol. 1975;121:933–941. [PMC free article] [PubMed]
43. Boethling R S. Regulation of extracellular protease secretion in Pseudomonas maltophilia. J Bacteriol. 1975;123:954–961. [PMC free article] [PubMed]
44. Bollet C, Davin-Regli A, De Micco P. A simple method for selective isolation of Stenotrophomonas maltophilia from environmental samples. Appl Environ Microbiol. 1995;61:1653–1654. [PMC free article] [PubMed]
45. Bonfiglio G, Livermore D M. Effect of media composition on the susceptibility of Xanthomonas maltophilia to beta-lactam antibiotics. J Antimicrob Chemother. 1991;28:837–842. [PubMed]
46. Bonfiglio G, Livermore D M. Zinc ions and medium-dependent susceptibility to beta-lactams in Xanthomonas maltophilia. J Antimicrob Chemother. 1994;33:181–183. [PubMed]
47. Bonfiglio G, Stefani S, Nicoletti G. Clinical isolate of a Xanthomonas maltophilia strain producing L1 deficient and L2 inducible β-lactamases. Chemotherapy. 1995;41:121–124. [PubMed]
48. Borowicz J J, Brishammar S, Gerhardson B. A Xanthomonas maltophilia isolate tolerating up to 1% sodium azide in Tris/HCl buffer. World J Microbiol Biotechnol. 1995;11:236–237. [PubMed]
49. Bottone E J, Madayag R M, Qureshi M N. Acanthamoeba keratitis: synergy between amebic and bacterial co-contaminants in contact lens care systems as a prelude to infection. J Clin Microbiol. 1992;30:2447–2450. [PMC free article] [PubMed]
50. Bottone E J, Perez A A, Gordon R F, Qureshi M N. Differential binding capacity and internalisation of bacterial substrates as factors in growth rate of Acanthamoeba spp. J Med Microbiol. 1994;40:148–154. [PubMed]
51. Bottone E J, Perez II A A, Oeser J L. Loofah sponges as reservoirs and vehicles in the transmission of potentially pathogenic bacterial species to human skin. J Clin Microbiol. 1994;32:469–472. [PMC free article] [PubMed]
52. Bottone E J, Reitano M, Janda J M, Troy K, Cuttner J. Pseudomonas maltophilia exoenzyme activity as a correlate in pathogenesis of ecthyma gangrenosum. J Clin Microbiol. 1986;24:995–997. [PMC free article] [PubMed]
53. Bradbury J F. Genus II. Xanthomonas. In: Krieg N R, Holt J G, editors. Bergey’s manual of systematic bacteriology. Vol. 1. Baltimore, Md: The Williams & Wilkins Co.; 1984. pp. 199–210.
54. British Thoracic Society Research Committee and the Public Health Laboratory Service. The aetiology, management, and outcome of severe community-acquired pneumonia on the intensive care unit. Respir Med. 1992;86:7–13. [PubMed]
55. Britt A J, Bruce N C, Lowe C R. Identification of a cocaine esterase in a strain of Pseudomonas maltophilia. J Bacteriol. 1992;174:2087–2094. [PMC free article] [PubMed]
56. Brooks, R. G., R. E. McCabe, K. L. Vosti, and J. S. Remington. 1985. Open trial of imipenem/cilastatin therapy for serious bacterial infections. Rev. Infect. Dis. 7(Suppl. 3):S496–S505. [PubMed]
57. Brown L L, Evelyn T P T, Iwama G K, Nelson W S, Levine R P. Bacterial species other than Renibacterium salmoninarum cross react with antisera against R. salmoninarum but are negative for the p57 gene of R. salmoninarum as detected by the polymerase chain reaction (PCR) Dis Aquat Org. 1995;21:227–231.
58. Bryson H M, Brogden R N. Piperacillin/tazobactam. A review of its antibacterial activity, pharmacokinetic properties, and therapeutic potential. Drugs. 1994;47:506–535. [PubMed]
59. Burdge D R, Noble M A, Campbell M E, Krell V L, Speert D P. 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;20:445–458. [PubMed]
60. Calandra, G. B., K. R. Brown, L. C. Grad, V. I. Ahonkai, C. Wang, and M. A. Aziz. 1985. Review of adverse experience and tolerability in the first 2,516 patients treated with imipenem/cilastatin. Am. J. Med. 78(Suppl. A):73–78. [PubMed]
61. Cameron J L, Reese W A, Tayal V S, Clark R F, Kelso D, Gonzalez E R, Garnett A R, Ornato J P. Bacterial contamination of ambulance oxygen humidifier water reservoirs: a potential source of pulmonary infection. Ann Emerg Med. 1986;15:1300–1302. [PubMed]
62. Canton E, Peman J, Jimenez M T, Ramon M S, Gobernado M. In vitro activity of sparfloxacin compared with those of five other quinolones. Antimicrob Agents Chemother. 1992;36:558–565. [PMC free article] [PubMed]
63. Carmeli, Y., and M. Samore. 1996. Imipenem and ceftazidime treatment as risk factors for nosocomial acquisition of Stenotrophomonas (Xanthomonas) maltophilia: a (sic) historical cohort study. Infect. Control Hosp. Epidemiol. 17(Suppl.):P31.
64. Carr H S, Wladowski T J, Rosenkranz H S. Silver sulfadiazine: in vitro antibacterial activity. Antimicrob Agents Chemother. 1973;4:585–587. [PMC free article] [PubMed]
65. Carrell D J, Hammond M E, Odell W D. Evidence for an autocrine/paracrine function of chorionic gonadotrophin in Xanthomonas maltophilia. Endocrinology. 1993;132:1085–1089. [PubMed]
66. Chan E L, Zabransky R J. Determination of synergy by two methods with eight antimicrobial combinations against tobramycin-susceptible and trobramycin-resistant strains of Pseudomonas. Diagn Microbiol Infect Dis. 1987;6:157–164. [PubMed]
67. Chatelut M, Dournes J L, Chabanon G, Marty N. Epidemiological typing of Stenotrophomonas (Xanthomonas) maltophilia by PCR. J Clin Microbiol. 1995;33:912–914. [PMC free article] [PubMed]
68. Chen S, Stroh E M, Wald K, Jalkh A. Xanthomonas maltophilia endophthalmitis after implantation of sustained-release ganciclovir. Am J Ophthalmol. 1992;15:772–773. [PubMed]
69. Cheng A F, Li M K W, Ling T K W, French G L. Emergence of ofloxacin-resistant Citrobacter freundii and Pseudomonas maltophilia after ofloxacin therapy. J Antimicrob Chemother. 1987;20:283–292. [PubMed]
70. Chester V, Cleary T J. Evaluation of the Minitek system for identification of nonfermentative and nonenteric fermentative gram-negative bacilli. J Clin Microbiol. 1980;12:509–516. [PMC free article] [PubMed]
71. Child J, Andrews J, Boswell F, Brenwald N, Wise R. The in vitro activity of CP99,219, a new naphthyridone antimicrobial agent: a comparison with fluoroquinolone agents. J Antimicrob Chemother. 1995;35:869–876. [PubMed]
72. Chow A W, Wong J, Bartlett K H. Synergistic interactions of ciprofloxacin and extended spectrum beta-lactams or aminoglycosides against multiply drug-resistant Pseudomonas maltophilia. Antimicrob Agents Chemother. 1988;32:782–784. [PMC free article] [PubMed]
73. Clark B J, Harkins L S, Munro F A, Devonshire P. Microbial contamination of cases used for storing contact lenses. J Infect. 1994;28:293–302. [PubMed]
74. Cohn R C, Jacobs M, Aronoff S C. In vitro activity of amiloride combined with tobramycin against Pseudomonas isolates from patients with cystic fibrosis. Antimicrob Agents Chemother. 1988;32:395–396. [PMC free article] [PubMed]
75. Cooke P, Heritage J, Kerr K, Hawkey P M, Newton K E. Different effects of zinc ions on in vitro susceptibilities of Stenotrophomonas maltophilia to imipenem and meropenem. Antimicrob Agents Chemother. 1996;40:2909–2910. [PMC free article] [PubMed]
76. Corbel M J, Stuart F A, Brewer R A. Observations on serological cross-reactions between smooth Brucella species and organisms of other genera. Dev Biol Stand. 1984;56:341–348. [PubMed]
77. Craven, D. E., K. A. Steger, and T. W. Barber. 1991. Preventing nosocomial pneumonia: state of the art and perspectives for the 1990s. Am. J. Med. 91(Suppl. 3B):44S–53S. [PubMed]
78. Crossley K, Matsen J M. Intravenous catheter-associated bacteremia: role of the diagnostic microbiology laboratory. Appl Microbiol. 1973;26:1006–1007. [PMC free article] [PubMed]
79. Cullmann W. Antibiotic susceptibility and outer membrane proteins of clinical Xanthomonas maltophilia isolates. Chemotherapy. 1991;37:246–250. [PubMed]
80. Cullmann W, Dick W. Heterogeneity of beta-lactamase production in Pseudomonas maltophilia: a nosocomial pathogen. Chemotherapy. 1990;36:117–126. [PubMed]
81. Daley C, Lim I, Modra J, Wilkinson I. Comparative evaluation of non-radiometric BACTEC and improved Oxoid Signal blood culture systems in a clinical laboratory. J Clin Microbiol. 1990;28:1586–1590. [PMC free article] [PubMed]
82. D’Amato R F, Thornsberry C, Baker C N, Kirven L A. Effect of calcium and magnesium ions on the susceptibility of Pseudomonas species to tetracycline, gentamicin, polymyxin B, and carbenicillin. Antimicrob Agents Chemother. 1975;7:596–600. [PMC free article] [PubMed]
83. Dapena F, Selgas R, Garcia-Perea A, Del Peso G, Bajo M A, Fernandez Reyes M J, Jimenez C, Sanchez C. Clinical significance of exit site infections due to Xanthomonas in CAPD patients: a comparison with Pseudomonas infection. Nephrol Dial Transplant. 1994;9:1774–1777. [PubMed]
84. Davin-Regli A, Bollet C, Auffray J P, Saux P, De Micco P. Use of random amplified polymorphic DNA for epidemiological typing of Stenotrophomonas maltophilia. J Hosp Infect. 1996;32:39–50. [PubMed]
85. Debette J, Blondeau R. Characterisation de bacteries tellurique assimables a Pseudomonas maltophilia. Can J Microbiol. 1977;23:1123–1127. [PubMed]
86. Debette J, Blondeau R. Presence de Pseudomonas maltophilia dans la rhizosphere de quelques plantes cultivees. Can J Microbiol. 1980;26:460–463. [PubMed]
87. Debette J, Prensier G. Immunoelectron microscopic demonstration of an esterase on the outer membrane of Xanthomonas maltophilia. Appl Environ Microbiol. 1989;55:233–239. [PMC free article] [PubMed]
88. Dembry, L. M., P. A. Farrell, D. R. Orcutt, L. A. Gerrity, and V. T. Andriole. 1997. In-vitro activity of trovafloxacin against sensitive and resistant aerobic bacteria using the standard microdilution broth method and Etest. J. Antimicrob. Chemother. 39(Suppl. B):35–42. [PubMed]
89. Demko C, Doershuk C, Stern R. Thirteen year experience with Xanthomonas maltophilia in patients with cystic fibrosis. Pediatr Pulmon Suppl. 1995;12:244. . (Abstract.)
90. Denis F, Sow A, David M, Chivon J P, Samb A, Mar I D. Meningites a Pseudomonas maltophilia. A propos de deux cas. Med Mal Infect. 1977;7:228–231.
91. Denton M. Stenotrophomonas maltophilia: an emerging problem in cystic fibrosis patients. Rev Med Microbiol. 1997;8:15–19.
92. Denton M, Hall M J, Todd N J, Littlewood J M. Abstracts of the 20th European Cystic Fibrosis Conference. 1995. A novel selective culture medium reveals a previously underestimated prevalence of Stenotrophomonas (Xanthomonas) maltophilia in a cystic fibrosis clinic, abstr. P14.
93. 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. [PubMed]
94. Denton M, Todd N J, Littlewood J M, Hawkey P M. Molecular typing of Stenotrophomonas maltophilia isolated from cystic fibrosis patients. J Infect. 1996;32:88.
95. Department of Health. Ice cubes: infection caused by Xanthomonas maltophilia. Hazard (93) 42. London, United Kingdom: Medical Services Directorate, Department of Health; 1993.
96. De Vos P, De Ley J. Intra- and intergeneric similarities of Pseudomonas and Xanthomonas ribosomal ribonucleic acid cistrons. Int J Syst Bacteriol. 1983;33:487–509.
97. Diaz-Mitoma, F., G. K. M. Harding, T. J. Louie, M. Thomson, M. James, and A. R. Ronald. 1985. Prospective randomized comparison of imipenem/cilastatin and cefotaxime for treatment of lung, soft tissue and renal infections. Rev. Infect. Dis. 7(Suppl. 3):S452–S457. [PubMed]
98. Di Fabio J L, Perry M B, Bundle D R. Analysis of the lipopolysaccharide of Pseudomonas maltophilia 555. Biochem Cell Biol. 1987;65:968–977. [PubMed]
99. Dirksen, M. S. C., R. G. F. Wintermans, J. B. J. Boerema, and J. S. F. Gimbrere. 1986. Imipenem as monotherapy in the treatment of intensive care patients with severe infections. J. Antimicrob. Chemother. 18(Suppl. E):145–151. [PubMed]
100. Dismukes W E, Karchmer A W, Buckley M J, Austen W G, Swartz M N. Prosthetic valve endocarditis. Circulation. 1973;48:365–377. [PubMed]
101. Dobbins J J, Johnson G S, Kunin C M, De Vries W C. Post-mortem microbiological findings of two artificial heart recipients. JAMA. 1988;259:865–869. [PubMed]
102. Doerr C A, Demmler G J, Garcia-Prats J A, Brandt M L. Solitary pyogenic liver abscess in neonates: report of three cases and review of the literature. Pediatr Infect Dis J. 1994;13:64–69. [PubMed]
103. Donzis P B, Mondino B J, Weissman B A, Bruckner D A. Microbial contamination of contact lens care systems. Am J Ophthalmol. 1987;104:325–333. [PubMed]
104. Drancourt M, Bollet C, Raoult D. Stenotrophomonas africana sp. nov., an opportunistic human pathogen in Africa. Int J Syst Bacteriol. 1997;47:160–163. [PubMed]
105. Draper C S, Walker R D, Lawler H E. Patterns of oral bacterial infection in captive snakes. J Am Vet Med Assoc. 1981;179:1223–1226. [PubMed]
106. Dufresne J, Vezina G, Levesque R C. Molecular cloning and expression of the imipenem-hydrolysing beta-lactamase gene from Pseudomonas maltophilia in Escherichia coli. Rev Infect Dis. 1988;10:806–817. [PubMed]
107. Durbec O, Albanese J, Brunel M F, Soula F, Granthil C. Septicemie foudroyante a Pseudomonas maltophilia au cours d’un traitement par imipeneme et amikacine. Presse Med. 1989;18:227–228. [PubMed]
108. Dutkiewicz J, Sorenson W G, Lewis D M, Olenchock S A. Levels of bacteria, fungi, and endotoxin in stored timber. Int J Biodeter Biodeg. 1992;30:29–41.
109. Dyte P H, Gillians J A. Pseudomonas maltophilia infection in an abattoir worker. Med J Aust. 1977;1:444–445. [PubMed]
110. Edinger R, Courtney R R, Hollick G E. Evaluation of the Pasco gram-negative non-fermenter identification system. Diagn Microbiol Infect Dis. 1994;19:61–63. [PubMed]
111. Edwards J R, Turner P J, Wannop C, Withnell E S, Grindley A J, Nairn K. In vitro anti-bacterial activity of SM-7338, a carbapenem antibiotic with stability to dehydropeptidase I. Antimicrob Agents Chemother. 1989;33:215–222. [PMC free article] [PubMed]
112. Elad Y, Koelh J, Fokkema N J. Control of infection and sporulation of Botrytis cinerea on bean and tomato by saprophytic bacteria and fungi. Eur J Plant Pathol. 1994;100:315–336.
113. Elkhaili H, Pompei D, Linger L, Kamili N, Monteil H, Jehl F. Cinetique de bactericidie de cefepime et cefpirome seuls ou associés a la gentamicine, amikacine ou ciprofloxacine sur Acinetobacter baumanii, Stenotrophomonas maltophilia et Enterobacter cloacae hyperproducteur de cephalosporinase. Pathol Biol. 1996;44:367–373. [PubMed]
114. El-Sweify M, Aly M F F. Polymerase chain reaction-based ribotyping of Pseudomonas maltophilia: a potential epidemiological marker. Infect Control Hosp Epidemiol. 1996;17:45.
115. Elting L S, Bodey G P. Septicaemia due to Xanthomonas species and non-aeruginosa Pseudomonas species: increasing incidence of catheter-related infections. Medicine. 1990;69:296–306. [PubMed]
116. 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. [PubMed]
117. Fabe C, Rodriguez P, Cony-Malchoul P, Parneix P, Bebear C, Mougein J. Typage moleculaire par electrophorese en champ pulse de souches de Stenotrophomonas maltophilia isolees dans un service d’hematologie. Pathol Biol. 1996;44:435–451. [PubMed]
118. Fang F C, Madinger N E. Resistant nosocomial gram-negative bacillary pathogens: Acinetobacter baumanii, Xanthomonas maltophilia, and Pseudomonas cepacia. Curr Top Infect Dis Clin Microbiol. 1996;116:52–83. [PubMed]
119. Fang G-D, Fine M, Orloff J, Arisumi D, Yu V L, Kapoor W, Grayston J T, Wang S P, Kohler R, Muder R R, Yee Y C, Rihs J D, Vickers R M. New and emerging etiologies for community-acquired pneumonia with implications for therapy: a prospective multi-center study of 359 cases. Medicine. 1990;69:307–316. [PubMed]
120. Farr B M, Karser D L, Harrison B D W, Connolly C K. Prediction of microbial aetiology at admission to hospital for pneumonia from the presenting clinical features. Thorax. 1989;44:1031–1035. [PMC free article] [PubMed]
121. Fass, R. J., J. Barnishan, M. C. Solomon, and L. W. Ayers. In vitro activities of quinolones, beta-lactams, tobramycin, and trimethoprim-sulfamethoxazole against non-fermentative gram-negative bacilli. Antimicrob. Agents Chemother. 40:1412–1418. [PMC free article] [PubMed]
122. Fass R J, Prior R B. Comparative in vitro activities of piperacillin-tazobactam and ticarcillin-clavulanate. Antimicrob Agents Chemother. 1989;33:1268–1272. [PMC free article] [PubMed]
123. Feeley T W, Du Moulin G C, Hedley-White J, Bushnell L S, Gilbert J P, Feingold D S. Aerosol polymyxin and pneumonia in seriously ill patients. N Engl J Med. 1975;293:471–475. [PubMed]
124. Felegie T P, Yu V L, Rumans L W, Yee R B. Susceptibility of Pseudomonas maltophilia to antimicrobial agents singly and in combination. Antimicrob Agents Chemother. 1979;16:833–837. [PMC free article] [PubMed]
125. Felici A, Amicosante G. Kinetic analysis of extension of substrate specificity with Xanthomonas maltophilia, Aeromonas hydrophila, and Bacillus cereus metallo-beta-lactamases. Antimicrob Agents Chemother. 1995;39:192–199. [PMC free article] [PubMed]
126. Felici A, Amicosante G, Oratore A, Strom R, Ledent P, Joris B, Fanuel L, Frere J-M. An overview of the kinetic parameters of class B beta-lactamases. Biochem J. 1993;291:151–155. [PMC free article] [PubMed]
127. Fenton J J, Harsch H H, Klein D. Production of volatile nitrogenous compounds from the degradation of streptomycin by Pseudomonas maltophilia. J Bacteriol. 1973;116:1267–1272. [PMC free article] [PubMed]
128. Fischer, J. J. 1973. Pseudomonas maltophilia endocarditis after replacement of the mitral valve: a case study. J. Infect. Dis. 128(Suppl.):S771–S773. [PubMed]
129. Fisher M C, Long S S, Roberts E M, Dunn J M, Balsara R K. Pseudomonas maltophilia bacteremia in children undergoing open heart surgery. JAMA. 1981;246:1571–1574. [PubMed]
130. Flaherty J P, Garcia-Houchins S, Chudy R, Arnow P M. An outbreak of gram-negative bacteremia traced to contaminated O-rings in reprocessed dialyzers. Ann Intern Med. 1993;119:1072–1078. [PubMed]
131. Ford A S, Baltch A L, Smith R P, Ritz W. In vitro susceptibilities of Pseudomonas aeruginosa and Pseudomonas spp. to the new fluoroquinolone clinafloxacin and PD 131628 and nine other antimicrobial agents. J Antimicrob Chemother. 1993;31:523–532. [PubMed]
132. Franzetti F, Cernuschi M, Esposito R, Moroni M. Pseudomonas infections in patients with AIDS and AIDS-related complex. J Intern Med. 1992;231:437–443. [PubMed]
133. Frederiksen B, Hoiby N, Koch C. Stenotrophomonas (Xanthomonas) maltophilia at the Danish Cystic Fibrosis Centre 1974–1993. Pediatr Pulmon Suppl. 1995;12:287. . (Abstract.)
134. Fritsche, D., R. Lutticken, and H. Bohmer. Pseudomonas maltophilia als Erreger menschlicher Infektionen. Zentralbl. Bakteriol. Mikrobiol. Hyg. Abt. 1 Orig. A 229:89–97. [PubMed]
135. Fritz M E, Eke P I, Malmquist J, Hardwick R. Clinical and microbiological observations of early polytetrafluoroethylene membrane exposure in guided bone regeneration. Case reports in primates. J Periodontol. 1996;67:245–249. [PubMed]
136. Fuchs P C, Barry A L, Pfaller M A. Antibacterial activity of PD 131628 and proposed disc diffusion susceptibility test criteria. J Antimicrob Chemother. 1994;33:1147–1154. [PubMed]
137. Fujita J, Yamadori I, Xu G, Hojo S, Negayama K, Miyawaki H, Yamaji Y, Takahara J. Clinical features of Stenotrophomonas maltophilia pneumonia in immunocompromised patients. Respir Med. 1996;90:35–38. [PubMed]
138. Ganadu M, Mura G L, Campus A M, Cherchi G L, Fanelli V, Calvisi L, Canu G, Cherchi G B. Relapsing pyrogenic reactions due to Xanthomonas maltophilia in a dialysis patient with a long-term central venous catheter. Nephrol Dial Transplant. 1996;11:197–198. [PubMed]
139. Garau, J., R. Martin, E. Bouza, J. Romero, J. A. Garcia-Rodriguez, E. Perea, F. Martinez Luengas, M. Gobernado, and R. Montero. 1986. Imipenem in the treatment of severe bacterial infections in seriously ill patients. J. Antimicrob. Chemother. 18(Suppl. E):131–140. [PubMed]
140. Garcia A, Sierra M F, Friberg J. Survival of bacteria after freezing of human semen in liquid nitrogen. Fertil Steril. 1981;35:549–551. [PubMed]
141. Garcia-Rodriguez J A, Fresnadillo M J, Garcia Garcia M I, Garcia Sanchez E, Garcia Sanchez J E, Trujillano I. the Spanish Study Group on Quinolone Resistance. Multicenter Spanish study of ciprofloxacin susceptibility in gram-negative bacteria. Eur J Clin Microbiol Infect Dis. 1995;14:456–459. [PubMed]
142. Garcia-Rodriguez J A, Garcia Sanchez J E, Garcia Garcia M I, Garcia Sanchez E, Munoz Bellido J L. Antibiotic susceptibility profile of Xanthomonas maltophilia: in vitro activity of beta-lactam/beta-lactamase inhibitor combinations. Diagn Microbiol Infect Dis. 1991;14:239–243. [PubMed]
143. Garcia-Rodriguez J A, Garcia Sanchez J E, Munoz Bellido J L, Garcia Garcia M I, Garcia Sanchez E. Kinetics of antimicrobial activity of aztreonam/clavulanic acid (2:1) against Xanthomonas maltophilia. J Antimicrob Chemother. 1991;27:552–554. [PubMed]
144. Garcia-Rodriguez J A, Garcia Sanchez J E, Munoz Bellido J L, Garcia Sanchez E, Garcia Garcia M I. In vitro activity of meropenem, a new carbapenem, against imipenem-resistant Pseudomonas aeruginosa and Xanthomonas maltophilia. J Chemother. 1991;3:143–146. [PubMed]
145. Gardner P, Griffin W B, Swartz M N, Kunz L J. Non-fermentative gram-negative bacilli of nosocomial interest. Am J Med. 1970;48:735–749. [PubMed]
146. Garrison M W, Anderson D E, Campbell D M, Carroll K C, Malone C L, Anderson J D, Hollis R J, Pfaller M J. Stenotrophomonas maltophilia: emergence of multidrug-resistant strains during therapy in an in vitro pharmacodynamic chamber model. Antimicrob Agents Chemother. 1996;40:2859–2864. [PMC free article] [PubMed]
147. Gerner-Smidt P, Bruun B, Arpi M, Schmidt J. Diversity of nosocomial Xanthomonas maltophilia (Stenotrophomonas maltophilia) as determined by ribotyping. Eur J Clin Microbiol Infect Dis. 1995;14:137–140. [PubMed]
148. Gilardi G L. Pseudomonas maltophilia infections in man. Am J Clin Pathol. 1969;51:58–61. [PubMed]
149. Gilardi G L. Characterization of nonfermentative nonfastidious gram-negative bacteria encountered in medical bacteriology. J Appl Bacteriol. 1971;34:623–644. [PubMed]
150. Gilardi G L. Infrequently encountered Pseudomonas species causing infection in humans. Ann Intern Med. 1972;77:211–215. [PubMed]
151. Gilardi G L. Non-fermentative gram-negative bacteria encountered in clinical specimens. Antonie Leeuwenhoek. 1973;39:229–242. [PubMed]
152. Gilardi G L. Pseudomonas species in clinical microbiology. Mount Sinai J Med. 1976;43:710–726. [PubMed]
153. Girijaratnakumari T, Raja A, Ramani R, Antony B, Shivananda P G. Meningitis due to Xanthomonas maltophilia. J Postgrad Med. 1993;39:153–155. [PubMed]
154. 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. [PMC free article] [PubMed]
155. Gordon G, Indeck M, Bross J, Kapoor D A, Brotman S. Injury from silage wagon accident complicated by mucormycosis. J Trauma. 1988;28:866–867. [PubMed]
156. Gould I M, Milne K. In-vitro pharmacodynamic studies of piperacillin/tazobactam with gentamicin and ciprofloxacin. J Antimicrob Chemother. 1997;39:53–61. [PubMed]
157. Goze A. Incidence des Pseudomonas sans pigment et des Moraxella en milieu hospitalier. Rev Epidemiol Med Sec Sante Publique. 1973;21:499–520.
158. Graham D Y, Yoshimura H H, Estes M K. DNA hybridization studies of the association of Pseudomonas maltophilia with inflammatory bowel disease. J Lab Clin Med. 1983;101:940–954. [PubMed]
159. Grant M M, Niedermann M S, Poehlmann M A, Fein A M. Characterisation of Pseudomonas aeruginosa adherence to cultured hamster tracheal epithelial cells. Am J Respir Cell Mol Biol. 1991;5:563–570. [PubMed]
160. Grehn M. Über die Toxizität einiger Spezies sog. nicht fermentativer gramnegativer Bakterien. Zentralbl Bakteriol Parasitenkd Infektranskr Hyg Abt I Orig Reihe A. 1976;235:84–89. [PubMed]
161. Grimard D, Bergeron M G. False resistance of Streptococcus faecalis and Pseudomonas maltophilia to norfloxacin by disc diffusion susceptibility testing. J Antimicrob Chemother. 1985;16:132–133. [PubMed]
162. Grover S, Odell W D. Partial characterisation of the 30 kD Ig-binding protein from Pseudomonas maltophilia. Biochem Biophys Res Commun. 1992;182:1075–1081. [PubMed]
163. Grover S, Odell W D. Characterisation of the 48.5 kDa chorionic gonadotrophin-like protein from Xanthomonas maltophilia. Endocr Res. 1993;19:147–162. [PubMed]
164. Grover S, Woodward S R, Caticha O, Carrell D T, Odell W D. Partial nucleotide sequence of the Xanthomonas maltophilia chorionic gonadotrophin-like receptor. Biochem Biophys Res Commun. 1993;190:371–376. [PubMed]
165. Grover S, Woodward S R, Odell W D. A bacterial protein has homology with human chorionic gonadotrophin (hCG) Biochem Biophys Res Commun. 1993;193:841–847. [PubMed]
166. Grover S, Woodward S R, Odell W D. Complete sequence of the gene encoding a chorionic gonadotrophin-like protein from Xanthomonas maltophilia. Gene. 1995;156:75–78. [PubMed]
167. Guerzoni M E, Lanciotti R, Sinigaglia M, Gardini F. Analysis of the interaction between autochthonous bacteria and packaging material in PVC-bottled mineral water. Microb Res. 1994;149:115–122. [PubMed]
168. Gutierrez Rodero F, del Mar Masia M, Cortes J, Ortiz de la Tabla V, Mainar V, Vilar A. Endocarditis caused by Stenotrophomonas maltophilia: case report and review. Clin Infect Dis. 1996;23:1261–1265. [PubMed]
169. Hardy D J, Hulbert B B, Migneault P C. Time to detection of positive BacT/Alert blood cultures and lack of need for routine subculture of 5- to 7-day negative cultures. J Clin Microbiol. 1992;30:2743–2745. [PMC free article] [PubMed]
170. Harlowe H D. Acute mastoiditis following Pseudomonas maltophilia infection. Laryngoscope. 1972;82:882–883. [PubMed]
171. Hawkey P M, Birkenhead D, Kerr K G, Newton K E, Hyde W A. Effect of divalent cations in bacteriological media in the susceptibility of Xanthomonas maltophilia to imipenem with special reference to zinc ions. J Antimicrob Chemother. 1993;31:47–55. [PubMed]
172. Heath T, Currie B. Nosocomial and community acquired Xanthomonas maltophilia infection in tropical Australia. J Hosp Infect. 1995;30:309–313. [PubMed]
173. Hebbar P, Berge O, Heulin T, Singh S P. Bacterial antagonists of sunflower (Helianthus annuus L.) fungal pathogens. Plant Soil. 1991;133:131–140.
174. Hellinger W C, Cawley J J, Alvarez S, Hogan S F, Harmsen W S, Ilstrup D M, Cockerill F R., III Clinical comparison of the Isolator and BacT/Alert aerobic blood culture systems. J Clin Microbiol. 1995;33:1787–1790. [PMC free article] [PubMed]
175. Henderson E, Ledgerwood, Hope K, Ross G, Krulicki W, Louie T. Screening and isolation for patients with multi-resistant organisms. Infect Control Hosp Epidemiol. 1996;17:30.
176. Hernandez-Duquino H, Rosenberg F A. Antibiotic-resistant Pseudomonas in bottled drinking water. Can J Microbiol. 1987;33:286–289. [PubMed]
177. Hirai Y. Survival of bacteria under dry conditions: from a viewpoint of nosocomial infection. J Hosp Infect. 1991;19:191–200. [PubMed]
178. Hohl P, Frei R, Aubry P. In vitro susceptibility of 33 clinical case isolates of Xanthomonas maltophilia: inconsistent correlation of agar dilution and of disk diffusion test results. Diagn Microbiol Infect Dis. 1991;14:447–450. [PubMed]
179. Holmes B, Costas M, Thaker T, Stevens M. Evaluation of two BBL Crystal systems for identification of some clinically important gram-negative bacilli. J Clin Microbiol. 1994;32:2221–2224. [PMC free article] [PubMed]
180. Holmes B, Lapage S P, Easterling B G. Distribution in clinical material and identification of Pseudomonas maltophilia. J Clin Pathol. 1979;32:66–72. [PMC free article] [PubMed]
181. Hoppe J E, Holzwarth I, Stern M. Comparison of four methods for pretreatment of cystic fibrosis sputum. Eur J Clin Microbiol Infect Dis. 1996;15:895–896. [PubMed]
182. Hosaka M, Yasue T, Fukuda H, Tomizawa H, Aoyama H, Hirai K. In vitro and in vivo antibacterial activities of AM-1155, a new 6-fluoro-8-methoxyquinolone. Antimicrob Agents Chemother. 1992;36:2108–2117. [PMC free article] [PubMed]
183. Hugh R, Gilardi G L. Pseudomonas. In: Lennette E H, Balows A, Hausler W Jr, Truant J P, editors. Manual of clinical microbiology. 3rd ed. Washington, D.C: American Society for Microbiology; 1980. pp. 288–317.
184. Hugh R, Leifson E. A description of the type strain of Pseudomonas maltophilia. Int Bull Bacteriol Nomencl Taxon. 1963;13:133–138.
185. Hugh R, Ryschenkow E. An Alcaligenes-like Pseudomonas species. Bacteriol. Proc. 1960. 1960. p. 78.
186. Hugh R, Ryschenkow E. Pseudomonas maltophilia, an Alcaligenes-like species. J Gen Microbiol. 1961;26:123–132. [PubMed]
187. Hulisz D T, File T M. Predisposing factors and antibiotic use in nosocomial infections caused by Xanthomonas maltophilia. Infect Control Hosp Epidemiol. 1992;13:489–490. [PubMed]
188. Hupkova M, Blahova J, Kralikova J, Krcmery V. Transferable resistance to beta-lactams in a nosocomial strain of Xanthomonas maltophilia. Antimicrob Agents Chemother. 1995;39:1011–1012. [PMC free article] [PubMed]
189. Ianinni, P. B., M. J. Kunkel, E. Hilton, and G. M. Ianinni. 1985. Imipenem/cilastatin: general experience in a community hospital. Am. J. Med. 78(Suppl. 6A):122–126. [PubMed]
190. Ibbotson J P, Pease P E, Allen R N. Serological studies in Crohn’s disease. Eur J Clin Microbiol. 1987;6:286–290. [PubMed]
191. Iizuka H, Komagata K. Microbiological studies on petroleum and natural gas. I. Determination of hydrocarbon-utilizing bacteria. J Gen Appl Microbiol. 1964;10:207–221.
192. Iizuka H, Komagata K. Taxonomy of the genus Pseudomonas with special reference to their modes of metabolism of carbon compounds. J Gen Appl Microbiol. 1963;9:83–95.
193. Ikemoto S, Suzuki K, Kaneko T, Komagata K. Characterization of strains of Pseudomonas maltophilia which do not require methionine. Int J Syst Bacteriol. 1980;30:437–447.
194. Irifune K, Ishida T, Shimoguchi K, Ohtake J, Tanaka T, Morikawa N, Kaku M, Koga H, Kohno S, Hara K. Pneumonia caused by Stenotrophomonas maltophilia with a mucoid phenotype. J Clin Microbiol. 1994;32:2856–2857. [PMC free article] [PubMed]
195. Jakobi M, Winkelmann G, Kaiser D, Kempler C, Jung G, Berg G, Bahl H. Maltophilin: a new antifungal compound produced by Stenotrophomonas maltophilia R3089. J Antibiot. 1996;49:1101–1104. [PubMed]
196. Janda J M, Bottone E J. Pathogenic properties and enzyme profiles of Pseudomonas and Acinetobacter. In: Gilardi G L, editor. Non-fermentative gram-negative rods: laboratory identification and clinical aspects. New York, N.Y: Marcel Dekker, Inc.; 1985. pp. 233–254.
197. Jang T-N, Wang F-D, Wang L-H, Liu C-Y, Liu I-M. Xanthomonas maltophilia bacteremia: an analysis of 32 cases. J Formosan Med Assoc. 1992;91:1170–1176. [PubMed]
198. Jones, R. N. 1995. Isepamicin (SCH 21420, 1-N-HAPA gentamicin B); microbiological characteristics including antimicrobial potency of spectrum of activity. J. Chemother. 7(Suppl. 2):7–16. [PubMed]
199. Jones R N, Erwin M E. In vitro activity of CP-74667 compared with four other fluoroquinolones. Diagn Microbiol Infect Dis. 1992;15:531–536. [PubMed]
200. Jucker B A, Harms H, Zehnder A J B. Adhesion of the positively charged bacterium Stenotrophomonas (Xanthomonas) maltophilia 70401 to glass and Teflon. J Bacteriol. 1996;178:5472–5479. [PMC free article] [PubMed]
201. Juffs H S. Identification of Pseudomonas species isolated from milk produced in South Eastern Queensland. J Appl Bacteriol. 1973;36:585–598. [PubMed]
202. Juhnke M E, Des Jardin E. Selective medium for isolation of Xanthomonas maltophilia from soil and rhizosphere environments. Appl Environ Microbiol. 1989;55:747–750. [PMC free article] [PubMed]
203. Juhnke M E, Mathre D E, Sands D C. Identification and characterization of rhizosphere competent bacteria of wheat. Appl Environ Microbiol. 1987;53:2793–2794. [PMC free article] [PubMed]
204. Kaiser G M, Tso P C, Morris R, McCurdy D. Xanthomonas maltophilia endophthalmitis after cataract extraction. Am J Ophthalmol. 1997;123:410–411. [PubMed]
205. Kampfer P, Dott W. Evaluation of the Titertek-NF system for identification of gram-negative bacteria. J Clin Microbiol. 1989;27:1201–1205. [PMC free article] [PubMed]
206. Karalus N C, Cursons R T, Leng R A, Mahood C B, Rothwell R P G, Hancock B, Cepulis S, Wawatai M, Coleman L. Community-acquired pneumonia: aetiology and prognostic index evaluation. Thorax. 1991;46:413–416. [PMC free article] [PubMed]
207. Karpati F, Malmborg A S, Alfredsson H, Hjelte L, Strandvik B. Bacterial colonisation with Xanthomonas maltophilia—a retrospective study in a cystic fibrosis patient population. Infection. 1994;22:258–263. [PubMed]
208. Kato N, Morioka T. Purpura fulminans secondary to Xanthomonas maltophilia sepsis in an adult with aplastic anaemia. J Dermatol. 1991;18:225–229. [PubMed]
209. Kawai F. Bacterial degradation of acrylic oligomers and polymers. Appl Microbiol Biotechnol. 1993;39:382–385.
210. Kealey G P, Cram A E. Pseudomonas maltophilia: an unusual burn wound pathogen. J Burn Care Rehab. 1986;7:409–410. [PubMed]
211. Kelly L D, Xu L-J. The effect of concurrent Pseudomonas or Xanthomonas exposure on adherence of Acanthamoeba castellani to soft contact lenses. Graefe’s Arch Clin Exp Ophthalmol. 1996;234:311–314. [PubMed]
212. Kelly M D, Mortensen J E, Konkle B A, Stull T L. A plasmid mediating production of a β-lactamase by Stenotrophomonas maltophilia. Curr Ther Res. 1995;56:152–162.
213. Kerr J R. Inhibition of growth of fungi pathogenic to man by Stenotrophomonas maltophilia. J Med Microbiol. 1996;45:380–382. [PubMed]
214. Kerr K G, Anson J, Hawkey P M. Abstracts of the 94th General Meeting of the American Society for Microbiology 1994. Washington, D.C: American Society for Microbiology; 1994. Adherence of clinical and environmental strains of Xanthomonas maltophilia to plastic material, abstr. B-339.
215. Kerr K G, Corps C M, Hawkey P M. Infections due to Xanthomonas maltophilia in patients with hematologic malignancy. Rev Infect Dis. 1991;13:762. [PubMed]
216. Kerr K G, Denton M, Todd N J, Corps C M, Kumari P, Hawkey P M. A novel selective culture medium for the isolation of Stenotrophomonas maltophilia. Eur J Clin Microbiol Infect Dis. 1996;15:607–610. [PubMed]
217. Kerr K G, Hawkey P M. Abstracts of the 2nd International Symposium on Febrile Neutropenia 1995. 1995. Serum resistance of clinical and environmental strains of Stenotrophomonas maltophilia, abstr. 29.
218. Kerr K G, Hawkey P M, Child J A, Norfolk D R, Anderson A W. Pseudomonas maltophilia infections in neutropenic patients and the use of imipenem. Postgrad Med J. 1990;66:1090. [PMC free article] [PubMed]
219. Kerr, K. G., and F. H. Wilkinson. Bottled water as a source of Stenotrophomonas maltophilia and Pseudomonas spp for neutropenic patients. Eur. J. Cancer Care, in press. [PubMed]
220. Khardori N, Elting L, Wong E, Schable B, Bodey G P. Nosocomial infections due to Xanthomonas maltophilia (Pseudomonas maltophilia) in patients with cancer. Rev Infect Dis. 1991;12:997–1003. [PubMed]
221. Khardori N, Reuben A, Rosenbaum B, Rolston K, Bodey G P. In vitro susceptibility of Xanthomonas (Pseudomonas) maltophilia to newer antimicrobial agents. Antimicrob Agents Chemother. 1990;34:1609–1610. [PMC free article] [PubMed]
222. Kiehn T E, Armstrong D. Changes in the spectrum of organisms causing bacteraemia and fungaemia in immunocompromised patients due to venous access devices. Eur J Clin Microbiol. 1990;9:869–872. [PubMed]
223. King A, Bethune L, Phillips I. The in vitro activity of levafloxacin compared with other antimicrobial agents. J Antimicrob Chemother. 1991;27:769–779. [PubMed]
224. King A, Bethune L, Phillips I. The in vitro activity of tosufloxacin, a new fluorinated quinolone compared with that of ciprofloxacin and temofloxacin. J Antimicrob Chemother. 1991;28:719–725. [PubMed]
225. King B A, Shannon K P, Phillips I. Aminoglycoside-6′-N-acetyltransferase production by an isolate of Pseudomonas maltophilia. J Antimicrob Chemother. 1978;4:467–468. [PubMed]
226. Kirkley B A, Easley K A, Basille B A, Washington J A. Controlled clinical comparison of two lysis-based blood culture systems, Isolator and Septi-Chek Release, for detection of bloodstream infections. J Clin Microbiol. 1993;31:2114–2117. [PMC free article] [PubMed]
227. Kirkley B A, Easley K A, Washington J A. Controlled clinical evaluation of Isolator and ESP aerobic blood culture systems for detection of bloodstream infections. J Clin Microbiol. 1994;32:1547–1549. [PMC free article] [PubMed]
228. Kiska D L, Kerr A, Jones M C, Caracciolo J A, Eskridge B, Jordan M, Miller S, Hughes D, King N, Gilligan P H. 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. [PMC free article] [PubMed]
229. Kitch T T, Jacobs M R, Applebaum P C. Evaluation of the 4-hour RapID NF Plus method for identification of 345 gram-negative nonfermentative rods. J Clin Microbiol. 1992;30:1267–1270. [PMC free article] [PubMed]
230. Klick J M, Du Moulin G C. An oxygen analyzer as a source of Pseudomonas. Anesthesiology. 1978;49:293–294. [PubMed]
231. Klinger J D, Thomassen M J. Occurrence and antimicrobial susceptibility of gram-negative non-fermentative bacilli in cystic fibrosis patients. Diagn Microbiol Infect Dis. 1985;3:149–158. [PubMed]
232. Kobayashi D Y, Guglielmoni M, Clarke B B. Isolation of the chitinolytic bacteria Xanthomonas maltophilia and Serratia marcescens as biological control agents for summer patch disease of turf grass. Soil Biol Biochem. 1995;27:1479–1487.
233. Kollef M H, Silver P, Murphy D M, Trouillon E. The effect of late-onset ventilator-associated pneumonia in determining patient mortality. Chest. 1995;108:1655–1662. [PubMed]
234. Komagata K. Differentiation of genus Pseudomonas and related aerobic bacteria. J Gen Appl Microbiol. 1961;7:282–299.
235. Komagata K, Yabuuchi Y, Tamagawa V, Ohyama A. Pseudomonas melanogena Iizuka and Komagata 1963, a later subjective synonym of Pseudomonas maltophilia Hugh and Ryschenkow 1960. Int J Syst Bacteriol. 1974;24:242–247.
236. Korn, C., R. Burke, C. O’Donnell, and E. Smail. 1996. An outbreak of Stenotrophomonas (Xanthomonas) maltophilia associated with reusable in-line ventilator temperature probes. Infect. Control Hosp. Epidemiol. 17(Suppl.):P48.
237. Krachmer J H, Purcell J J. Bacterial corneal ulcers in cosmetic soft contact lens wearers. Arch Ophthalmol. 1978;96:57–61. [PubMed]
238. Krcmery V, Jr, Pichna P, Oravcova E, Lacka J, Kukuckova E, Studena M, Grausova S, Stopkova K, Krupova I. Stenotrophomonas maltophilia bacteraemia in cancer patients: report on 31 cases. J Hosp Infect. 1996;34:75–77. [PubMed]
239. Kwok O C H, Fahy P C, Hoitink H A J, Kuter G A. Interactions between bacteria and Trichoderma hamatum in suppression of Rhizoctonia damping-off in bark compost media. Phytopathology. 1987;77:1206–1212.
240. Labows J N, McGinley K J, Webster G F, Leyden J J. Headspace analysis of volatile metabolites of Pseudomonas aeruginosa and related species by gas chromatography-mass spectrometry. J Clin Microbiol. 1980;12:521–526. [PMC free article] [PubMed]
241. Laing F P Y, Ramotar K, Read R R, Alfieri N, Kureishi A, Henderson E A, Louie T J. Molecular epidemiology of Xanthomonas maltophilia colonization and infection in the hospital environment. J Clin Microbiol. 1995;33:513–518. [PMC free article] [PubMed]
242. Lambert B, Beyns F, Van Rooyen L, Gossele F, Papon Y, Swings J. Rhizobacteria of maize and their antifungal activities. Appl Environ Microbiol. 1987;53:1866–1871. [PMC free article] [PubMed]
243. Lambert B, Meire P, Joos H, Lens P, Swings J. Fast-growing aerobic heterotrophic bacteria from the rhizosphere of young sugar beet plants. Appl Environ Microbiol. 1990;56:3375–3381. [PMC free article] [PubMed]
244. Lee N A, Clark D P. A natural isolate of Pseudomonas maltophilia which degrades aromatic sulfonic acids. FEMS Microbiol Lett. 1993;107:151–155. [PubMed]
245. Lee N-R, Hwang M-O, Jung G-H, Kim Y-S, Min K-H. Physical structure and expression of alkBA encoding alkane hydroxylase and rubredoxin reductase from Pseudomonas maltophilia. Biochem Biophys Res Commun. 1996;218:17–21. [PubMed]
246. Lesco-Bornet M, Pierre J, Sarkis-Karam D, Lubera S, Bergogne-Berezin E. Susceptibility of Xanthomonas maltophilia to six quinolones and study of outer membrane proteins in resistant mutants selected in vitro. Antimicrob Agents Chemother. 1992;36:669–671. [PMC free article] [PubMed]
247. Liaw Y S, Yang P C, Wu Z G, Yu C J, Chang D B, Lee L N, Kuo S H, Luh K T. The bacteriology of obstructive pneumonitis: a prospective study using ultrasound-guided transthoracic needle aspiration. Am J Respir Crit Care Med. 1994;149:1648–1653. [PubMed]
248. Litopoulou-Tzanetaki E, Vafopoulou-Mastrojiannaki A. Hydrolase activities of whole cells and crude cell-free extract of gram-negative isolates from refrigerated raw ewe milk. Milchwissenschaft. 1995;50:610–614.
249. Liu P Y-F, Lau Y-J, Hu B-S, Shyr J-M, Shi Z-Y, Tsai W-S, Lin Y-H, Tseng C-Y. Comparison of susceptibility to extended-spectrum β-lactam antibiotics and ciprofloxacin among gram-negative bacilli isolated from intensive care units. Diagn Microbiol Infect Dis. 1995;22:285–291. [PubMed]
250. Lookingbill D P, Miller S H, Knowles R C. Bacteriology of chronic leg ulcers. Arch Dermatol. 1978;114:1765–1768. [PubMed]
251. Louie A, Baltch A L, Ritz W J, Smith R P. Comparative in vitro susceptibilities of Pseudomonas aeruginosa, Xanthomonas maltophilia, and Pseudomonas species to sparfloxacin, CI-978, AT4140, PD131501, and reference antimicrobial agents. J Antimicrob Chemother. 1991;27:793–799. [PubMed]
252. Lysenko O, Weiser J. Bacteria associated with the nematode Neoaplectana carpocapsae and the pathogenicity of this complex for Galleria mellonella larvae. J Invertebr Pathol. 1974;24:332–336. [PubMed]
253. MacDiarmid J A, Burrell D H. Degradation of the wool fibre by bacteria isolated from fleece rot. Wool Technol Sheep Breed. 1993;40:123–126.
254. Maes M. Fast classification of plant-associated bacteria in the Xanthomonas genus. FEMS Microbiol Lett. 1993;113:161–166.
255. Malecka-Griggs B, Reinhardt D J. Direct dilution sampling, quantitation, and microbial assessment of open-system ventilation circuits in intensive care units. J Clin Microbiol. 1983;17:870–877. [PMC free article] [PubMed]
256. Manian F A, Meyer L, Jenne J, Owen A, Taff T. Loss of antimicrobial susceptibility in aerobic gram-negative bacilli repeatedly isolated from patients in intensive care units. Infect Control Hosp Epidemiol. 1996;17:222–226. [PubMed]
257. Maningo E, Watanakunakorn C. Xanthomonas maltophilia and Pseudomonas cepacia in lower respiratory tracts of patients in critical care units. J Infect. 1995;31:89–92. [PubMed]
258. Margesin R, Schinner F. Characterization of a metalloprotease from psychrophilic Xanthomonas maltophilia. FEMS Microbiol Lett. 1991;79:257–261.
259. Markowitz S M, Williams D S, Hanna C B, Parker J L, Pierce M A, Steele J C., Jr A multi-center comparative study of the in vitro activity of fleroxacin and other antibacterial agents. Chemotherapy. 1995;41:477–486. [PubMed]
260. Marraro R V, Mitchell J L. Exogenous methionine requirements of Pseudomonas maltophilia. J Am Med Technol. 1974;36:239–240.
261. Marrie T J, Durrant H, Yates L. Community-acquired pneumonia requiring hospitalisation: five year prospective study. Rev Infect Dis. 1989;11:586–599. [PubMed]
262. Marshall W F, Keating M R, Anhalt J P, Steckelberg J M. Xanthomonas maltophilia: an emerging nosocomial pathogen. Mayo Clin Proc. 1989;64:1097–1104. [PubMed]
263. Martin R, Siavoshi F, McDougal D L. Comparison of RapID NFT system and conventional methods for identification of nonsaccharolytic gram-negative bacteria. J Clin Microbiol. 1986;24:1089–1092. [PMC free article] [PubMed]
264. Mazzola M, Stahlman P W, Leach J E. Application method affects the distribution and efficacy of rhizobacteria suppressive of downy brome (Bromus tectorum) Soil Biol Biochem. 1995;27:1271–1278.
265. McDonald G R, Pernenkil R. Community-acquired Xanthomonas maltophilia pyelonephritis. South Med J. 1993;86:967–968. [PubMed]
266. McKee K T, Melly M A, Greene H L, Schaffner W. Gram-negative bacillary sepsis associated with use of lipid emulsion in parenteral nutrition. Am J Dis Child. 1979;133:649–650. [PubMed]
267. Meier S, Zellweger G, Elsner P, Wurthrich D, Krause M. Purpura fulminans bei Morbus Still und Bakteriamie mit Xanthomonas maltophilia und koagulase negativen Staphylokokken. Schweiz Med Wochenschr. 1994;124:900–905. [PubMed]
268. Metchock B, Thornsberry C. Susceptibility of Xanthomonas (Pseudomonas) maltophilia to antimicrobial agents: methodological problems. Antimicrob Newsl. 1989;6:35–40.
269. Mett H, Rosta S, Schacher B, Frei R. Outer membrane permeability and beta-lactamase content in Pseudomonas maltophilia clinical isolates and laboratory mutants. Rev Infect Dis. 1988;10:765–769. [PubMed]
270. Midelfart J, Midelfart A, Bevanger L. Microbial contamination of contact lens cases among medical students. CLAO J. 1996;22:21–24. [PubMed]
271. Miller J M, Rhoden D L. Preliminary evaluation of Biolog, a carbon source utilization method for bacterial identification. J Clin Microbiol. 1991;29:1143–1147. [PMC free article] [PubMed]
272. Minah G E, Rednor J L, Peterson D E, Overholser C D, Depaola L G, Suzuki J B. Oral succession of gram-negative bacilli in myelosuppressed cancer patients. J Clin Microbiol. 1986;24:210–213. [PMC free article] [PubMed]
273. Mirgain I, Green G A, Monteil H. Degradation of atrazine in laboratory microcosms: isolation and identification of the biodegrading bacteria. Environ Toxicol Chem. 1993;12:1627–1634.
274. Moffet H L, Allan D, Williams T. Survival and dissemination of bacteria in nebulisers and incubators. Am J Dis Child. 1967;114:13–20. [PubMed]
275. Moffet H L, Williams T. Bacteria recovered from distilled water and inhalation equipment. Am J Dis Child. 1967;114:7–11. [PubMed]
276. Moody M R, Young V M. In vitro susceptibility of Pseudomonas cepacia and Pseudomonas maltophilia to trimethoprim and trimethoprim-sulfamethoxazole. Antimicrob Agents Chemother. 1975;7:836–839. [PMC free article] [PubMed]
277. Moody M R, Young V M, Kenton D M. In vitro antibiotic susceptibility of Pseudomonads other than Pseudomonas aeruginosa recovered from cancer patients. Antimicrob Agents Chemother. 1972;2:344–349. [PMC free article] [PubMed]
278. Morello J A, Leitch C, Nitz S, Dyke J W, Andruszewski M, Maier G, Landau W, Beard M A. Detection of bacteremia by Difco ESP blood culture system. J Clin Microbiol. 1994;32:811–818. [PMC free article] [PubMed]
279. Morrison A J, Jr, Hoffmann K K, Wenzel R P. Associated mortality and clinical characteristics of nosocomial Pseudomonas maltophilia in a university hospital. J Clin Microbiol. 1986;24:52–55. [PMC free article] [PubMed]
280. Mortensen J E, Fisher M C, LiPuma J J. Recovery of Pseudomonas cepacia and other Pseudomonas species from the environment. Infect Control Hosp Epidemiol. 1995;16:30–32. [PubMed]
281. Moss C W, Samuels S B, Liddle J, McKinney R M. Occurrence of branched chain hydroxy fatty acids in Pseudomonas maltophilia. J Bacteriol. 1973;114:1018–1025. [PMC free article] [PubMed]
282. Moss C W, Samuels S B, Weaver R E. Cellular fatty acid composition of selected Pseudomonas species. Appl Microbiol. 1972;24:596–598. [PMC free article] [PubMed]
283. Moss R B. Cystic fibrosis: pathogenesis, pulmonary infection, and treatment. Clin Infect Dis. 1995;21:839–851. [PubMed]
284. Muder R R, Harris A P, Muller S, Edmond M, Chow J W, Papadakis K, Wagener M W, Bodey G P, Steckelberg J M. Bacteremia due to Stenotrophomonas (Xanthomonas) maltophilia: a prospective multi-center study of 91 episodes. Clin Infect Dis. 1996;22:508–512. [PubMed]
285. Muder R R, Yu V L, Dummer J S, Vinson C, Lumish R M. Infections caused by Pseudomonas maltophilia: expanding clinical spectrum. Arch Intern Med. 1987;147:1672–1674. [PubMed]
286. Munoz J L, Garcia M I, Munoz S, Leal S, Fajardo M, Garcia-Rodriguez J A. Activity of trimethoprim/sulfamethoxazole plus polymyxin B against multiresistant Stenotrophomonas maltophilia. Eur J Clin Microbiol Infect Dis. 1996;15:879–882. [PubMed]
287. Nagai T. Association of Pseudomonas maltophilia with malignant lesions. J Clin Microbiol. 1984;20:1003–1005. [PMC free article] [PubMed]
288. Nakatsu C H, Fulthorpe R R, Holland B A, Peel M C, Wyndham R C. The phylogenetic distribution of a transposable dioxygenase from the Niagara River watershed. Mol Ecol. 1995;4:593–603. [PubMed]
289. Narasimhan S L, Gopaul D L, Hatch L A. Pseudomonas maltophilia bacteremia associated with a prolapsed mitral valve. Am J Clin Pathol. 1977;68:304–306. [PubMed]
290. National Committee for Clinical Laboratory Standards. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard M7-A4. Villanova, Pa: National Committee for Clinical Laboratory Standards; 1997.
291. Nawaz M S, Franklin W, Cerniglia C E. Degradation of acrylamide by immobilised cells of a Pseudomonas sp. and Xanthomonas maltophilia. Can J Microbiol. 1993;39:207–212. [PubMed]
292. Neal D J, Wilkinson S G. Lipopolysaccharides from Pseudomonas maltophilia: structural studies of the side chain, core, and lipid A regions of the lipopolysaccharide from strain NCTC 10257. Eur J Biochem. 1982;128:143–149. [PubMed]
293. Nesme X, Vaneechoutte M, Orso S, Hoste B, Swings J. Diversity and genetic relatedness within genera Xanthomonas and Stenotrophomonas using restriction endonuclease site differences of PCR-amplified 16S rRNA gene. Syst Appl Microbiol. 1995;18:127–135.
294. Neu H, Saha G, Chin N. Resistance of Xanthomonas maltophilia to antibiotics and the effect of β-lactamase inhibitors. Diagn Microbiol Infect Dis. 1991;12:283–285. [PubMed]
295. Nguyen M H, Muder R R. Meningitis due to Xanthomonas maltophilia: case report and review. Clin Infect Dis. 1994;19:325–326. [PubMed]
296. Noble R C, Parekh M C. In vitro comparison of ceftazidime, aztreonam, cefpirome, gentamicin, imipenem, enoxacin, and ticarcillin plus clavulanic acid against 108 strains of Pseudomonas maltophilia. Curr Microbiol. 1987;15:177–179.
297. Nolte F S, Williams J M, Jerris R C, Morello J A, Leitch C D, Matushek S, Schwabe L D, Dorigan F, Kocka F E. Multicenter clinical evaluation of a continuous monitoring blood culture system using fluorescent-sensor technology (BACTEC 9240) J Clin Microbiol. 1993;31:552–557. [PMC free article] [PubMed]
298. Nord C-E, Sjoberg L, Wadstrom T, Wretlind B. Characterization of three Aeromonas and nine Pseudomonas species by extracellular enzymes and haemolysins. Med Microbiol Immunol. 1975;161:79–87. [PubMed]
299. Nord C-E, Wadstrom T, Wretlind B. Synergistic effect of combinations of sulfamethoxazole, trimethoprim, and colistin against Pseudomonas maltophilia and Pseudomonas cepacia. Antimicrob Agents Chemother. 1974;6:521–523. [PMC free article] [PubMed]
300. Nord C-E, Wadstrom T, Wretlind B. Antibiotic sensitivity of two Aeromonas and nine Pseudomonas species. Med Microbiol Immunol. 1975;161:89–97. [PubMed]
301. Noskin G A, Grohmann S M. Xanthomonas maltophilia bacteremia: an analysis of factors influencing outcome. Infect Dis Clin Pract. 1992;1:230–236.
302. O’Brien M, Davis G H G. Fibrinolysis as an aid in the identification of Pseudomonas species. Microbios Lett. 1981;16:41–43.
303. O’Brien M, Davis G H. Enzymatic profile of Pseudomonas maltophilia. J Clin Microbiol. 1982;16:417–421. [PMC free article] [PubMed]
304. O’Hara C M, Tenover F C, Miller J M. Parallel comparison of accuracy of API 20E, Vitek GNI, MicroScan Walk/Away Rapid ID, and Becton Dickinson Cobas Micro ID-E/NF for identification of members of the family Enterobacteriaceae and common gram-negative, non-glucose-fermenting bacilli. J Clin Microbiol. 1993;31:3165–3169. [PMC free article] [PubMed]
305. Oie S, Kamiya A. Microbial contamination of brushes used for pre-operative shaving. J Hosp Infect. 1992;21:103–110. [PubMed]
306. Olsen P E, Rice W A, Bordeleau L M, Demidoff A H, Collins M M. Levels and identities of nonrhizobial microorganisms found in commercial legume inoculant made with non-sterile peat carrier. Can J Microbiol. 1996;42:72–75. [PubMed]
307. Omri A, Ravaoarinoro M. Preparation, properties, and the effects of amikacin, netilmicin, and tobramycin in free and liposomal formulations on gram-negative and gram-positive bacteria. Int J Antimicrob Agents. 1996;7:9–14. [PubMed]
308. Orr K, Gould F K, Sisson P R, Lightfoot N F, Freeman R, Burdess D. Rapid inter-strain comparison by pyrolysis mass spectrometry in nosocomial infection with Xanthomonas maltophilia. J Hosp Infect. 1991;17:187–195. [PubMed]
309. Orrison L H, Bibb W F, Cherry W B, Thacker L. Determination of antigenic relationships among legionellae and non-legionellae by direct fluorescent-antibody and immunodiffusion tests. J Clin Microbiol. 1983;17:332–337. [PMC free article] [PubMed]
310. Osterhout G J, Shull V H, Dick J D. Identification of clinical isolates of gram-negative nonfermentative bacteria by an automated cellular fatty acid identification system. J Clin Microbiol. 1991;29:1822–1830. [PMC free article] [PubMed]
311. Oyiazu H, Komagata K. Grouping of Pseudomonas species on the basis of cellular fatty acid compositions and the quinone system with special reference to the existence of 3-hydroxy fatty acids. J Gen Appl Microbiol. 1983;29:17–40.
312. Palleroni N J. Genus I. Pseudomonas Migula 1894. In: Krieg N R, Holt J G, editors. Bergey’s manual of systematic bacteriology. Vol. 1. Baltimore, Md: The Williams & Wilkins Co.; 1984. pp. 141–199.
313. 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. [PubMed]
314. Palleroni N J, Kunisawa R, Contopoulou R, Doudoroff M. Nucleic acid homologies in the genus Pseudomonas. Int J Syst Bacteriol. 1973;23:333–339.
315. Pankuch G A, Jacobs M R, Applebaum P C. Susceptibilities of 123 Xanthomonas maltophilia strains to clinafloxacin, PD131628, PD138312, PD140248, ciprofloxacin, and ofloxacin. Antimicrob Agents Chemother. 1994;38:369–370. [PMC free article] [PubMed]
316. Pankuch G A, Jacobs M R, Rittenhouse S F, Applebaum P C. Susceptibilities of 123 strains of Xanthomonas maltophilia to eight β-lactams (including β-lactam–β-lactamase inhibitor combinations) and ciprofloxacin tested by five methods. Antimicrob Agents Chemother. 1994;38:2317–2322. [PMC free article] [PubMed]
317. Papadakis K A, Vartivarian S E, Vassilaki M E, Anaissie E J. Stenotrophomonas maltophilia: an unusual cause of biliary sepsis. Clin Infect Dis. 1995;21:1032–1034. [PubMed]
318. Papadakis K A, Vartivarian S E, Vassilaki M E, Anaissie E J. Septic pre-patellar bursitis caused by Stenotrophomonas (Xanthomonas) maltophilia. Clin Infect Dis. 1996;22:388–389. [PubMed]
319. Papapetropolou M, Iliopolou J, Rodopolou G, Detorakis J, Paniara O. Occurrence and antibiotic resistance of Pseudomonas species isolated from drinking water in southern Greece. J Chemother. 1994;6:111–116. [PubMed]
320. Papapetropolou M, Rodopolou G, Giannoulaki E, Stergiopoulos P. Effect of temperature on antimicrobial susceptibilities of Pseudomonas species isolated from drinking water. J Chemother. 1994;6:404–407. [PubMed]
321. Parent K, Mitchell P D. Bacterial variants: etiological agent in Crohn’s disease. Gastroenterology. 1976;71:365–368. [PubMed]
322. Parent K, Mitchell P. Cell wall-defective variants of Pseudomonas-like (group Va) bacteria in Crohn’s disease. Gastroenterology. 1978;75:368–372. [PubMed]
323. Parr M D, Bertch K E, Rapp R P. Amino-acid stability and microbial growth in total parenteral nutrient solutions. Am J Hosp Pharm. 1985;42:2688–2691. [PubMed]
324. Pasadakis P, Thodis E, Eftimimiadou A, Panagoutsos S, Papazoglou D, Kaliengidou M, Kartali S, Vargemezis V. Treatment and prevention of relapses of CAPD Pseudomonas peritonitis. Adv Periton Dial. 1993;9:206–210. [PubMed]
325. Pasargiklian I, Lusco G, Paizis G, Mascheroni E. Ticarcillin/clavulanic acid: determination of minimal inhibitory concentrations against bacterial strains isolated from intensive care units. Comparison with other strains. J Chemother. 1995;8:113–121. [PubMed]
326. Paton R, Miles R S, Amyes S G B. Biochemical properties of inducible β-lactamases produced from Xanthomonas maltophilia. Antimicrob Agents Chemother. 1994;38:2143–2149. [PMC free article] [PubMed]
327. Patrick S, Hindmarch J M, Hague R V, Harris D M. Meningitis caused by Pseudomonas maltophilia. J Clin Pathol. 1975;28:741–743. [PMC free article] [PubMed]
328. Payne D J, Bateson J H, Gasson B C, Proctor D, Khushi T, Farmer T H, Tolson D A, Bell D, Skett P W, Marshall A C, Reid R, Ghosez L, Combret Y, Marchand-Brynaert J. Inhibition of metallo-β-lactamases by a series of mercaptoacetic acid thiol ester derivatives. Antimicrob Agents Chemother. 1997;41:135–140. [PMC free article] [PubMed]
329. Payne D J, Cramp R, Bateson J H, Neale J, Knowles D. Rapid identification of metallo- and serine beta-lactamases. Antimicrob Agents Chemother. 1994;38:991–996. [PMC free article] [PubMed]
330. Pedersen M M, Marso E, Pickett J. Non-fermentative bacilli associated with man. III. Pathogenicity and antibiotic susceptibility. Am J Clin Pathol. 1970;54:178–192. [PubMed]
331. Penland R L, Wilhemus K R. Stenotrophomonas maltophilia ocular infections. Arch Ophthalmol. 1996;114:433–436. [PubMed]
332. Pfaller M A, Sahm D, O’Hara C, Ciaglia C, Yu M, Yamane N, Scharnweber G, Rhoden D. Comparison of the autoSCAN-W/A rapid bacterial identification system and the Vitek AutoMicrobic system for identification of gram-negative bacilli. J Clin Microbiol. 1991;29:1422–1428. [PMC free article] [PubMed]
333. Phale P S, Mahajan M C, Vaidyanathan C S. A pathway for biodegradation of 1-naphthoic acid by Pseudomonas maltophilia CSU89. Arch Microbiol. 1995;163:42–47. [PubMed]
334. Pham B N, Aractingi S, Dombret H, Arlet G, Hunault M, Degos L. Xanthomonas (formerly Pseudomonas) maltophilia-induced cellulitis in a neutropenic patient. Arch Dermatol. 1992;128:702–704. [PubMed]
335. Phillips I, King B A, Shannon K P. The mechanisms of resistance to aminoglycosides in the genus Pseudomonas. J Antimicrob Chemother. 1978;4:121–129. [PubMed]
336. Piddock L J, Turner H L. Activity of meropenem against imipenem-resistant bacteria and selection in vitro of carbapenem-resistant Enterobacteriaceae. Eur J Clin Microbiol Infect Dis. 1992;11:1186–1191. [PubMed]
337. Pitt T L. Burnt offerings or typing system. J Hosp Infect. 1991;17:157–158.
338. Pohlman J K, Kirkley B A, Easley K A, Basille B A, Washington J A. Controlled clinical evaluation of BACTEC Plus Aerobic/F and BacT/Alert Aerobic FAN bottles for detection of bloodstream infections. J Clin Microbiol. 1995;33:2856–2858. [PMC free article] [PubMed]
339. Pohlman J K, Kirkley B A, Easley K A, Washington J A. Controlled clinical comparison of Isolator and BACTEC 9240 Aerobic/F Resin bottle for detection of bloodstream infections. J Clin Microbiol. 1995;33:2525–2529. [PMC free article] [PubMed]
340. Poulos C D, Matsumura S O, Willey B M, Low D E, McGeer A. In vitro activities of antimicrobial combinations against Stenotrophomonas (Xanthomonas) maltophilia. Antimicrob Agents Chemother. 1995;39:2220–2223. [PMC free article] [PubMed]
341. Pradahananga S L, Rowling P J E, Simpson I N, Payne D J. Sensitivity of L2-type beta-lactamases from Stenotrophomonas maltophilia to serine active site beta-lactamase inhibitors. J Antimicrob Chemother. 1996;37:394–396. [PubMed]
342. Public Health Laboratory Service. Ice as a source of infection acquired in hospital. CDR Weekly. 1993;3:53.
343. Puckey D J, Norris J R, Gutteridge C S. Discrimination of micro-organisms using direct probe mass spectrometry. J Gen Microbiol. 1980;118:535–538. [PubMed]
344. Qadri S M H, Abo-Askar H, Veno Y. Antibacterial activity of the new quinolone CI-960 (PD127391) against clinical isolates at a major tertiary care center in Saudi Arabia. Chemotherapy (Basel) 1992;38:92–98. [PubMed]
345. Qadri S M H, Veno Y, Burns J V, Almodovar E, Rabea N. In vitro activity of sparfloxacin (CI-978), a new broad spectrum fluoroquinolone. Chemotherapy (Basel) 1992;38:99–106. [PubMed]
346. Qadri S M H, Veno Y, Saldin H, Burdette J M, Lee G C. Comparative antibacterial activity of the new fluoroquinolone PD 131628. Drug Invest. 1992;4:409–415.
347. Rahmati-Bahram A, Magee J T, Jackson S K. Growth temperature-dependent variation of cell-envelope lipids and antibiotic susceptibility in Stenotrophomonas (Xanthomonas) maltophilia. J Antimicrob Chemother. 1995;36:317–326. [PubMed]
348. Rahmati-Bahram A, Magee J T, Jackson S K. Temperature-dependent aminoglycoside resistance in Stenotrophomonas (Xanthomonas) maltophilia: alterations in protein and lipopolysaccharide with growth temperature. J Antimicrob Chemother. 1996;37:665–676. [PubMed]
349. Rahmati-Bahram A, Magee J T, Jackson S K. Effect of temperature on aminoglycoside binding sites in Stenotrophomonas maltophilia. J Antimicrob Chemother. 1997;39:19–24. [PubMed]
350. Ravizzola G, Pizzi R, Pirali F, Turano A. In vitro antibacterial activity of the new quinolone Bay y3118 against clinical isolates. J Chemother. 1994;6:392–398. [PubMed]
351. Rello J, Quintana E, Ausina V, Castella J, Luquin M, Net A, Prats G. Incidence, etiology, and outcome of nosocomial pneumonia in mechanically ventilated patients. Chest. 1991;100:439–444. [PubMed]
352. Rhoden D L, Schable B, Smith P B. Evaluation of PASCO MIC-ID system for identifying gram-negative bacilli. J Clin Microbiol. 1987;25:2363–2366. [PMC free article] [PubMed]
353. Richert N D, Ryan R J. Specific gonadotrophin binding to Pseudomonas maltophilia. Proc Natl Acad Sci USA. 1977;74:878–882. [PMC free article] [PubMed]
354. Ringertz S, Bjorklind A, Kronvall G. Species-specific interpretive breakpoints for ciprofloxacin disk diffusion susceptibility testing. Scand J Infect Dis Suppl. 1989;60:46–53. [PubMed]
355. Rivera J O, Lutomski D M. Co-trimoxazole use for resistant Pseudomonas maltophilia. Clin Pharm. 1984;3:308–311. [PubMed]
356. Robinson A, McCarter Y S, Tetreault J. Comparison of Crystal Enteric/Nonfermenter system, API 20E system, and Vitek AutoMicrobic system for identification of gram-negative bacilli. J Clin Microbiol. 1995;33:364–370. [PMC free article] [PubMed]
357. Rohner P, Pepey B, Auckenthaler R. Comparison of BacT/Alert with Signal blood culture system. J Clin Microbiol. 1995;33:313–317. [PMC free article] [PubMed]
358. Roilides E, Butler K M, Husson R N, Mueller B V, Lewis L L, Pizzo P A. Pseudomonas infections in children with HIV infection. Pediatr Infect Dis J. 1992;11:547–553. [PubMed]
359. Rolston K V I, Anaissie E A, Bodey G P. In vitro susceptibility of Pseudomonas species to fifteen antimicrobial agents. J Antimicrob Chemother. 1987;19:193–196. [PubMed]
360. Rolston, K. V. I., D. H. Ho, B. LeBlanc, H. Streeter, and T. Dvorak. 1997. In-vitro activity of trovafloxacin against clinical bacterial isolates from patients with cancer. J. Antimicrob. Chemother. 39(Suppl. B):15–22. [PubMed]
361. Rolston K V I, Messer M, Ho D H. Comparative in vitro activities of newer quinolones against Pseudomonas species and Xanthomonas maltophilia isolated from patients with cancer. Antimicrob Agents Chemother. 1990;34:1812–1813. [PMC free article] [PubMed]
362. Rosenblatt J E, Stewart P R. Combined activity of sulfamethoxazole, trimethoprim and polymyxin B against gram-negative bacilli. Antimicrob Agents Chemother. 1974;6:84–92. [PMC free article] [PubMed]
363. Rosenthal S L. Sources of Pseudomonas and Acinetobacter species found in human culture. Am J Clin Pathol. 1974;62:807–811. [PubMed]
364. Rosta S, Mett H. Physiological studies of the regulation of β-lactamase expression in Pseudomonas maltophilia. J Bacteriol. 1989;171:483–487. [PMC free article] [PubMed]
365. Roupas A, Pitton J S, Waldvogel F A. Influence de la temperature sur l’activite de la gentamycine chez Pseudomonas maltophilia. Schweiz Rundsch Med Prax. 1973;62:436–440. [PubMed]
366. Rouse, M. S., B. M. Tallan, N. K. Henry, J. M. Steckelberg, and W. R. Wilson. 1991. Treatment of Xanthomonas maltophilia experimental pneumonia. Chest 12(Suppl.):147S.
367. Sader H S, Jones R N. Antimicrobial activity of the new carbapenem biapenem compared to imipenem, meropenem and other broad spectrum beta-lactam drugs. Eur J Clin Microbiol Infect Dis. 1993;12:384–391. [PubMed]
368. Sader H S, Jones R N, Allen S D, Gerlach E H, Murray P R, Washington J A. In vitro comparison of activity of PC-17116, a new fluoroquinolone against more than 5000 recent clinical isolates from five medical centers. J Chemother. 1993;5:283–288. [PubMed]
369. Sader H S, Pignatari A C, Frei R, Hollis R J, Jones R N. Pulsed-field gel electrophoresis of restriction-digested genomic DNA and antimicrobial susceptibility of Xanthomonas maltophilia strains from Brazil, Switzerland, and the USA. J Antimicrob Chemother. 1994;33:615–618. [PubMed]
370. Saino Y, Inoue M, Mitsuhashi S. Purification and properties of an inducible cephalosporinase from Pseudomonas maltophilia GN12873. Antimicrob Agents Chemother. 1984;25:362–365. [PMC free article] [PubMed]
371. Saino Y, Kobayashi F, Inoue M, Mitsuhashi S. Purification and properties of inducible penicillin β-lactamase isolated from Pseudomonas maltophilia. Antimicrob Agents Chemother. 1982;22:564–570. [PMC free article] [PubMed]
372. Sarkar T K, Gilardi G, Aguam A S, Josephson J, Leventhal G. Primary Pseudomonas maltophilia infection of the lung. Postgrad Med. 1979;65:253–256. , 260. [PubMed]
373. Sarvamangala-Devi J N, Venkatesh A, Shivanandra P G. Neonatal infections due to Pseudomonas maltophilia. Indian Pediatr. 1984;21:72–73. [PubMed]
374. Schable B, Rhoden D L, Hugh R, Weaver R E, Khardori N, Smith P B, Bodey G P, Anderson R L. Serological classification of Xanthomonas maltophilia (Pseudomonas maltophilia) based on heat-stable O antigens. J Clin Microbiol. 1989;27:1011–1014. [PMC free article] [PubMed]
375. Schable B, Rhoden D L, Jarvis W R, Miller J M. Prevalence of serotypes of Xanthomonas maltophilia from worldwide sources. Epidemiol Infect. 1992;108:337–341. [PMC free article] [PubMed]
376. Schable B, Villarino M E, Favero M S, Miller J M. Application of multilocus enzyme electrophoresis to epidemiologic investigations of Xanthomonas maltophilia. Infect Control Hosp Epidemiol. 1991;12:163–167. [PubMed]
377. Scharmann W. Vorkommen von elatase bei Pseudomonas und Aeromonas. Zentralbl Bakteriol Microbiol Hyg 1 Abt Orig A. 1972;220:435–442. [PubMed]
378. Semel J D, Trenholme G M, Harris A A, Jupa J E, Levin S. Pseudomonas maltophilia pseudosepticaemia. Am J Med. 1978;64:403–406. [PubMed]
379. Sequeira W, Jones E, Siegel M E, Lorenz M, Kallick C. Pyogenic infections of the symphysis pubis. Ann Intern Med. 1982;96:604–606. [PubMed]
380. Shen P, Huang M, Peng Z. Studies of plasmids of Pseudomonas maltophilia. Acta Genet Sin. 1992;19:355–361. [PubMed]
381. Sierra M, Garcia-Lopez M L, Gonzalez E, Garcia M C, Otero O. Species of psychrotrophic bacteria on freshly-dressed lamb carcasses. Arch Lebensmittelhyg. 1995;46:20. , 22–23.
382. Sikorowski P P, Powell J E, Lawrence A M. Effects of bacterial contamination on development of Micropolitis croceipes. Entomophaga. 1992;37:475–481.
383. Singer E, Debette J, Lepretre A, Swings J. Comparative esterase electrophoretic polymorphism and phenotypic analysis of Xanthomonas maltophilia and related strains. Syst Appl Microbiol. 1994;17:387–394.
384. Smit W J, Boquest A L, Geddes J E, Tosolini F A. The antibiotic susceptibilities of Xanthomonas maltophilia and their relation to clinical management. Pathology. 1994;26:321–324. [PubMed]
385. Smith S M, Cundy K R, Gilardi G L, Wang W. Evaluation of the AutoMicrobic system for identification of glucose-nonfermenting gram-negative rods. J Clin Microbiol. 1982;15:302–307. [PMC free article] [PubMed]
386. Snyder M E, Katz H R. Ciprofloxacin-resistant bacterial keratitis. Am J Ophthalmol. 1992;114:336–338. [PubMed]
387. Sogaard P, Gahrn-Hansen B, Hui-Ping Z, Frederiksen W. An investigation of three commercial methods for rapid identification of non-enteric gram-negative rods. Acta Pathol Microbiol Immunol Scand Sect B. 1986;94:357–363. [PubMed]
388. Sonnenwirth A C. Bacteremia with and without meningitis due to Yersinia enterocolitica, Edwardsiella tarda, Comamonas terrigena, and Pseudomonas maltophilia. Ann N Y Acad Sci. 1970;174:488–502. [PubMed]
389. Soriano V, Valencia E, Alba A, Gonzalez-Lahoz J. Endocarditis por Xanthomonas maltophilia en un paciente con SIDA. Med Clin. 1994;102:399. [PubMed]
390. Southern P M, Jr, Schneider M L. Pseudomonas maltophilia in clinical bacteriologic specimens. Texas Rep Biol Med. 1974;32:880.
391. Spangler S K, Visalli M A, Jacobs M R, Applebaum P C. Susceptibilities of non-Pseudomonas aeruginosa gram-negative non-fermentative rods to ciprofloxacin, ofloxacin, levofloxacin, d-ofloxacin, sparfloxacin, ceftazidime, piperacillin, piperacillin-tazobactam, trimethoprim-sulfamethoxazole, and imipenem. Antimicrob Agents Chemother. 1996;40:772–775. [PMC free article] [PubMed]
392. Spencer, R. C. 1995. The emergence of epidemic, multiple-antibiotic-resistant Stenotrophomonas (Xanthomonas) maltophilia and Burkholderia (Pseudomonas) cepacia. J. Hosp. Infect. 30(Suppl.):453–464. [PubMed]
393. Spraul C W, Lang G E, Lang G K. Xanthomonas maltophilia keratitis associated with contact lenses. CLAO J. 1996;22:158. [PubMed]
394. Staneck J L, Weckbach L S, Tilton R C, Zabransky R J, Bayola-Mueller L, O’Hara C M, Miller J M. Collaborative evaluation of the Radiometer Sensititre AP80 for identification of gram-negative bacilli. J Clin Microbiol. 1993;31:1179–1184. [PMC free article] [PubMed]
395. Stanier R Y, Palleroni N J, Doudoroff M. The aerobic pseudomonads: a taxonomic study. J Gen Microbiol. 1966;43:159–271. [PubMed]
396. Stevens C M, Swaine D, Butler C, Carr A H, Weightman A, Catchpole C R, Healing D E, Elliott T S J. Development of o.a.s.i.s., a new automated blood culture system in which detection is based on measurement of bottle headspace pressure changes. J Clin Microbiol. 1994;32:1750–1756. [PMC free article] [PubMed]
397. Strandberg D A, Jorgensen J H, Drutz D J. Activities of aztreonam and new cephalosporins against infrequently isolated gram-negative bacilli. Antimicrob Agents Chemother. 1983;24:282–286. [PMC free article] [PubMed]
398. Su J J, Kafkewitz D. Utilization of toluene and xylenes by a nitrate-reducing strain of Pseudomonas maltophilia under low oxygen and anoxic conditions. FEMS Microbiol Ecol. 1994;15:249–257.
399. Subbannayya K, Ramnarayan K, Shivananda P G, Shatapathy P, Mathai P. Pseudomonas maltophilia endocarditis. Indian J Pathol Microbiol. 1984;27:311–315. [PubMed]
400. Suga K, Kabashima T, Ito K, Tsuru D, Okamura H, Kataoka J, Yoshimoto T. Prolidase from Xanthomonas maltophilia: purification and characterization of the enzyme. Biosci Biotechnol Biochem. 1995;59:2087–2090. [PubMed]
401. Sutter V L. Identification of Pseudomonas species isolated from hospital environment and human sources. Appl Microbiol. 1968;16:1532–1538. [PMC free article] [PubMed]
402. 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.
403. Szeto C C, Li P K, Leung C B, Yu A W, Lui S F, Lai K N. Xanthomonas maltophilia peritonitis in uremic patients receiving continuous ambulatory peritoneal dialysis. Am J Kidney Dis. 1997;29:91–95. [PubMed]
404. Taber T E, Hegeman T F, York S M, Kinney R A, Webb D H. Treatment of Pseudomonas infections in peritoneal dialysis patients. Periton Dial Int. 1991;11:213–216. [PubMed]
405. Talon D, Bailly P, Leprat R, Godard C, Deconnink E, Cahn J-Y, Michel-Briand Y. Typing of hospital strains of Xanthomonas maltophilia by pulsed-field gel electrophoresis. J Hosp Infect. 1994;27:209–217. [PubMed]
406. Tanaka M, Hohmura M, Nishi T, Sato K, Hayakawa H. Antimicrobial activity of DU-6681a, a parent compound of the novel carbapenem DZ-2640. Antimicrob Agents Chemother. 1997;41:1260–1268. [PMC free article] [PubMed]
407. Tenover F C, Mizuki T S, Carlson L G. Evaluation of autoSCAN-W/A automated microbiology system for the identification of non-glucose-fermenting gram-negative bacilli. J Clin Microbiol. 1990;28:1628–1634. [PMC free article] [PubMed]
408. Tilton R C, Steingrimsson O, Ryan R W. Susceptibilities of Pseudomonas species to tetracycline, minocycline, gentamicin, and tobramycin. Am J Clin Pathol. 1978;69:410–413. [PubMed]
409. Todd N J, Kerr K G, Denton M, Hawkey P M. Abstracts of the 92nd General Meeting of the American Society for Microbiology 1992. Washington, D.C: American Society for Microbiology; 1992. Extracellular enzyme activity of clinical and environmental strains of Xanthomonas maltophilia, abstr. L18.
410. Toledo-Pereyra L H, Raij L, Simmons R L, Najarian J S. Role of endotoxin and bacteria in long term survival of preserved small bowel allografts. Surgery. 1974;73:474–481. [PubMed]
411. Torres A, Aznar R, Gateil J M, Jimenez P, Gonzalez J, Ferrer A, Celis R, Rodriguez-Roisin R. Incidence, risk, and prognosis factors of nosocomial pneumonia in mechanically ventilated patients. Am Rev Respir Dis. 1990;142:523–528. [PubMed]
412. Townsend R, Winstanley T G, Spencer R C. In vitro susceptibility of Xanthomonas maltophilia to aztreonam and clavulanic acid as a test for the presumptive identification of the species. J Hosp Infect. 1991;18:324–325. [PubMed]
413. Traub W H, Spohr M. Comparative disk and broth dilution susceptibility test results with ticarcillin and timentin against Pseudomonas aeruginosa and Pseudomonas maltophilia. Chemotherapy. 1987;33:340–346. [PubMed]
414. Trumbore, D., R. Pontzer, M. E. Levinson, D. Kaye, M. Cynamon, C. Liu, D. R. Hinthorn, J. S. Tan, and T. M. File. 1985. Multicenter study of the clinical efficiency of imipenem/cilastatin for treatment of serious infections. Rev. Infect. Dis. 7(Suppl. 3):S476–S480. [PubMed]
415. Trump D L, Grossman S A, Thompson G, Murray K. CSF infections complicating the management of neoplastic meningitis: clinical features and results of therapy. Arch Intern Med. 1982;142:583–586. [PubMed]
416. Turner-Hubbard, K., W. K. Hadley, J. L. Gerberding, H. F. Chambers, and F. Perdreau-Remington. 1996. Bronchoscope sterilization failure causing contamination of bronchoalveolar lavage with Xanthomonas (Stenotrophomonas) maltophilia. Infect. Control Hosp. Epidemiol. 17(Suppl.):P43.
417. Tyler S D, Strathdee C A, Rozee K R, Johnson W M. Oligonucleotide primers designed to differentiate pathogenic pseudomonads on the basis of sequencing of genes coding for 16S-22S rRNA internal transcribed spacers. Clin Diagn Lab Immunol. 1995;2:448–453. [PMC free article] [PubMed]
418. Ulrich J A, Needham G M. Differentiation of Alcaligenes faecalis from Bordetella bronchisepticus [sic] by biochemical and nutritional methods. J Bacteriol. 1953;65:210–215. [PMC free article] [PubMed]
419. Van Couwenberghe C, Cohen S. Analysis of epidemic and endemic isolates of Xanthomonas maltophilia by contour clamped homogeneous electric field gel electrophoresis. Infect Control Hosp Epidemiol. 1994;15:691–696. [PubMed]
420. Van Couwenberghe C J, Cohen S H, Tang Y J, Gumerlock P H, Silva J., Jr Genomic fingerprinting of epidemic and endemic strains of Stenotrophomonas maltophilia (formerly Xanthomonas maltophilia) by arbitrarily primed PCR. J Clin Microbiol. 1995;33:1289–1291. [PMC free article] [PubMed]
421. Van den Mooter M, Swings J. Numerical analysis of 295 phenotypic features of 266 Xanthomonas strains and related strains and an improved taxonomy of the genus. Int J Syst Bacteriol. 1990;40:348–369. [PubMed]
422. Vanholder R, Vanhaecke E, Ringoir S. Pseudomonas septicemia due to deficient disinfectant mixing during reuse. Int J Artific Org. 1992;15:19–24. [PubMed]
423. Vanhoof R, Sonck P, Hannecart-Pokorni E. The role of lipopolysaccharide anionic binding sites in aminoglycoside uptake in Stenotrophomonas (Xanthomonas) maltophilia. J Antimicrob Chemother. 1995;35:167–171. [PubMed]
424. Van Zyl E, Steyn P L. Differentiation of phytopathogenic Pseudomonas and Xanthomonas species and pathovars by numerical taxonomy and protein gel electrophoresis. Syst Appl Microbiol. 1990;13:60–71.
425. Van Zyl E, Steyn P L. Reinterpretation of the taxonomic position of Xanthomonas maltophilia and taxonomic criteria in this genus. Request for an opinion. Int J Syst Bacteriol. 1992;42:193–198. [PubMed]
426. Varettas K, Mukerjee C, Schmidt M. A comparative study of the BBL Crystal Enteric/Nonfermenter identification system and the BioMerieux API 20E and API 20NE identification systems after overnight incubation. Pathology. 1996;27:358–361. [PubMed]
427. Vartivarian S, Anaissie E, Bodey G, Sprigg H, Rolston K. A changing pattern of susceptibility of Xanthomonas maltophilia to antimicrobial agents: implications for therapy. Antimicrob Agents Chemother. 1994;38:624–627. [PMC free article] [PubMed]
428. Vartivarian S E, Papadakis K A, Anaissie E J. Stenotrophomonas (Xanthomonas) maltophilia urinary tract infection. Arch Intern Med. 1996;156:433–435. [PubMed]
429. Vartivarian S E, Papadakis K A, Palacios J A, Manning J T, Anaissie E J. Mucocutaneous and soft tissue infections caused by Xanthomonas maltophilia: a new spectrum. Arch Intern Med. 1994;121:969–973. [PubMed]
430. Vazquez S C, Merino L N R, MacCormack W P, Fraile E R. Protease-producing psychrotrophic bacteria isolated from Antarctica. Polar Biol. 1995;15:131–135.
431. Veys A, Callewaert W, Waelkens E, van den Abbele K. Application of gas-liquid chromatography to the routine identification of nonfermenting gram-negative bacteria in clinical specimens. J Clin Microbiol. 1989;27:1538–1542. [PMC free article] [PubMed]
432. Victor M A, Arpi M, Bruun B, Jonsson V, Hansen M M. Xanthomonas maltophilia bacteremia in immunocompromised hematological patients. Scand J Infect Dis. 1994;26:163–170. [PubMed]
433. Villarino M E, Stevens L E, Schable B, Mayers G, Miller J M, Burke J P, Jarvis W R. Risk factors for epidemic Xanthomonas maltophilia infection/colonisation in intensive care unit patients. Infect Control Hosp Epidemiol. 1992;13:201–206. [PubMed]
434. Visalli M, Bajaksouzian S, Jacobs M, Appelbaum P. Program and Abstracts of the 36th Interscience Conference on Antimicrobial Agents and Chemotherapy. Washington, D.C: American Society for Microbiology; 1996. Activity of trovafloxacin alone and combined with ceftazidime, imipenem and amikacin against gram-negative nonfermenters; p. E86.
435. Visser M R, Bogaards L, Rozenberg-Arska M, Verhoef J. Comparison of the autoSCAN-W/A and Vitek AutoMicrobic systems for identification and susceptibility testing of bacteria. Eur J Clin Microbiol Infect Dis. 1992;11:979–984. [PubMed]
436. Von Graevenitz A, Bucher C. Isolation of Pseudomonas maltophilia from human stools with thienamycin. Zentralbl Bakteriol Mikrobiol Hyg I Abt Orig A. 1983;254:403–404. [PubMed]
437. Vu-Thein H, Moissenet D, Valcin M, Dulot C, Tournier G, Garberg-Chenon A. Molecular epidemiology of Burkholderia cepacia, Stenotrophomonas maltophilia and Alcaligenes xylosoxidans in a cystic fibrosis center. Eur J Clin Microbiol Infect Dis. 1996;15:876–878. [PubMed]
438. Wagn P, Hansen H M, Duun P S, Kolmos H J. Xanthomonas maltophilia arsag til epidural absces has en patient med epiduralkateter. Ugeskr Laeg. 1994;156:7229–7230. [PubMed]
439. Walsh T R, Hall L, Assinder S J, Nichols W W, Cartwright S J, MacGowan A P, Bennett P M. Sequence analysis of the L1 metallo-beta-lactamase from Xanthomonas maltophilia. Biochim Biophys Acta. 1994;1218:199–201. [PubMed]
440. Walsh T R, MacGowan A P, Bennett P M. Program and Abstracts of the 36th Interscience Conference on Antimicrobial Agents and Chemotherapy. Washington, D.C: American Society for Microbiology; 1996. Sequence analysis of the L2 serine β-lactamase from Stenotrophomonas maltophilia, abstr. C33.
441. Wauters G, Boel A, Voorn G P, Verhaegen J, Meunier F, Janssens M, Verbist L. Evaluation of a new identification system, Crystal Enteric/Non-Fermenter, for gram-negative bacilli. J Clin Microbiol. 1995;33:845–849. [PMC free article] [PubMed]
442. Wheat P F, Winstanley T G, Spencer R C. Effect of temperature on antimicrobial susceptibilities of Pseudomonas maltophilia. J Clin Pathol. 1985;38:1055–1058. [PMC free article] [PubMed]
443. Whorwell P J, Davidson I W, Beeken W L, Wright R. Search by immunofluorescence for antigens of rotavirus, Pseudomonas maltophilia, and Mycobacterium kansasii in Crohn’s disease. Lancet. 1978;ii:697–698. [PubMed]
444. Whorwell P J, Graham J, Machin D, Wright R. Lymphocyte transformation to specific antigens associated with Crohn’s disease. Hepato-Gastroenterol. 1981;28:258–260. [PubMed]
445. Widjojoatmodjo M N, Fluit A C, Verhoef J. Rapid identification of bacteria by PCR-single strand conformation polymorphism. J Clin Microbiol. 1994;32:3002–3007. [PMC free article] [PubMed]
446. Wilcox M H, Winstanley T G, Spencer R C. Outer membrane protein profiles of Xanthomonas maltophilia isolates displaying temperature-dependent susceptibility to gentamicin. J Antimicrob Chemother. 1994;33:663–666. [PubMed]
447. Wilkinson K G, Dixon K W, Sivasithamparam K, Ghisalberti E L. Effect of IAA on symbiotic germination of an Australian orchid and its production by orchid associated bacteria. Plant Soil. 1994;159:1291–1295.
448. Wilkinson S G, Galbraith L, Anderton W J. Lipopolysaccharides from Pseudomonas maltophilia: composition of the lipopolysaccharide and structure of the side-chain polysaccharide from strain N.C.I.B. 9204. Carbohydr Res. 1983;112:241–252. [PubMed]
449. Winn A M, Galbraith L, Temple G S, Wilkinson S G. Structure of the O19 antigen of Xanthomonas maltophilia. Carbohydr Res. 1993;247:249–254. [PubMed]
450. Winn A M, Miles C T, Wilkinson S G. Structure of the O3 antigen of Stenotrophomonas (Xanthomonas) maltophilia. Carbohydr Res. 1996;282:149–156. [PubMed]
451. Winn A M, Miller A W, Wilkinson S G. Structure of the O10 antigen of Stenotrophomonas (Xanthomonas) maltophilia. Carbohydr Res. 1995;267:127–133. [PubMed]
452. Winn A M, Wilkinson S G. Structure of the O6 antigen of Stenotrophomonas (Xanthomonas or Pseudomonas) maltophilia. Carbohydr Res. 1995;272:225–230. [PubMed]
453. Winston D J, Ho W G, Bruckner D A, Champlin R E. Beta-lactam therapy in febrile granulocytopenic patients. A randomized trial comparing cefoperazone plus piperacillin, ceftazidime plus piperacillin, and imipenem alone. Ann Intern Med. 1991;115:849–859. [PubMed]
454. Wise R, Andrews J M, Brenwald N. In vitro activity of the tricyclic β-lactam GV104326. Antimicrob Agents Chemother. 1996;40:1248–1253. [PMC free article] [PubMed]
455. Wishart M M, Riley T V. Infection with Pseudomonas maltophilia: hospital outbreak due to contaminated disinfectant. Med J Aust. 1976;2:710–712. [PubMed]
456. Witchitz S, Regnier B, Witchitz J, Schlemmer B, Bouvet E, Vachan F. Les endocardites a bacilles gram negatif. Pathol Biol. 1982;30:569–575. [PubMed]
457. Wood, M. E., and A. C. Newland. 1986. Intravenous ciprofloxacin in the treatment of infection in immunocompromised patients. J. Antimicrob. Chemother. 18(Suppl. D):175–178. [PubMed]
458. Wust J, Frei R, Gunthard H, Altwegg M. Analysis of restriction fragment length polymorphism and ribotyping of multiresistant Stenotrophomonas maltophilia isolated from persisting lung infection in a cystic fibrosis patient. Scand J Infect Dis. 1995;27:499–502. [PubMed]
459. Yamazaki E, Ishii J, Sato K, Nakae T. The barrier function of the outer membrane of Pseudomonas maltophilia in the diffusion of saccharides and beta-lactam antibiotics. FEMS Microbiol Lett. 1989;60:85–88. [PubMed]
460. Yang P, Vauterin L, Vancanneyt M, Swings J, Kersters K. Application of fatty acid methyl esters for the taxonomic analysis of the genus Xanthomonas. Syst Appl Microbiol. 1993;16:47–71.
461. Yang P, de Vos P, Kersters K, Swings J. Polyamine patterns as chemotaxonomic markers for the genus Xanthomonas maltophilia. Int J Syst Bacteriol. 1993;43:709–714.
462. Yao J D C, Conly J M, Krajden M. Molecular typing of Stenotrophomonas (Xanthomonas) maltophilia by DNA macrorestriction analysis and random amplified polymorphic DNA analysis. J Clin Microbiol. 1995;33:2195–2198. [PMC free article] [PubMed]
463. Yao J D C, Louie M, Louie L, Goodfellow J, Simor A E. Comparison of E test and agar dilution for antimicrobial susceptibility testing of Stenotrophomonas (Xanthomonas) maltophilia. J Clin Microbiol. 1995;33:1428–1430. [PMC free article] [PubMed]
464. Yeh T J, Anabtawi I N, Cornett V E, White A, Stern W H, Ellison R G. Bacterial endocarditis following open heart surgery. Ann Thorac Surg. 1967;3:29–36. [PubMed]
465. Yousem S A. Graft eosinophilia in lung transplantation. Hum Pathol. 1992;23:1172–1177. [PubMed]
466. Yu V L, Felegie T P, Yee R B, Pasculle A W, Taylor F H. Synergistic interaction in vitro with use of three antibiotics simultaneously against Pseudomonas maltophilia. J Infect Dis. 1980;142:602–607. [PubMed]
467. Yu V L, Rumans L W, Wing E J, McLeod R, Sattler F N, Harvey R M, Deresinski S C. Pseudomonas maltophilia causing heroin-associated infective endocarditis. Arch Intern Med. 1978;138:1667–1671. [PubMed]
468. Zechman J M, Labows J N. Volatiles of Pseudomonas aeruginosa and related species by automated headspace concentration gas chromatography. Can J Microbiol. 1985;31:232–237. [PubMed]
469. Zhong W P. Identification and classification of 204 strains of gram-negative organisms isolated from poultry eggs. Chin J Prev Med. 1990;24:257–260. . (In Chinese.) [PubMed]
470. Zuravleff J J, Yu V L. Infections caused by Pseudomonas maltophilia with emphasis on bacteremia: case reports and review of the literature. Rev Infect Dis. 1982;4:1236–1246. [PubMed]

Articles from Clinical Microbiology Reviews are provided here courtesy of American Society for Microbiology (ASM)
PubReader format: click here to try

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...