Q J Med 2003; 96: 227-234
© 2003 Association of Physicians
Bacteraemia in adults due to glucose non-fermentative Gram-negative bacilli other than P. aeruginosa
From the Departments of Infectious Diseases and 1 Microbiology, ICII, IDIBAPS, Hospital Clínic Universitari, Barcelona, Spain, and Departments of 2 Internal Medicine and 3 Epidemiology & Preventive Medicine, Hospital Universitari de Tarragona Joan XXIII, Universitat Rovira i Virgili, Tarragona, Spain
Received 7 August 2002 Accepted for publication 30 December 2002.
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Summary |
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Background: Glucose non-fermentative Gram-negative bacilli other than P. aeruginosa (NF) are emerging pathogens.
Aim: To evaluate the epidemiology, clinical characteristics, predictors of acquisition, and outcome of bacteraemia due to NF.
Design: Retrospective analysis of prospectively recorded data.
Methods: We reviewed episodes of NF bacteraemia in patients older than 14 years, recorded through a blood culture surveillance program. Patients were identified at the time of their bacteraemia and prospectively followed.
Results: Between January 1991 and December 2000, 296 episodes of NF bacteraemia were detected: 87% were due to Acinetobacter sp., Pseudomonas sp. other than P. aeruginosa, or Stenotrophomonas maltophilia. The global incidence (0.87 cases per 1000 discharges) remained stable during the study period. Patients were of all ages and both sexes, and 282/296 (95.3%) had some predisposing underlying disease or condition, the most common being haematological malignancies without transplantation (85/296, 28.7%), treatment with steroids (78/296, 26.3%), and transplantation (bone marrow or solid organ) (70/296, 23.6%). Fifty (16.9%) were neutropenic. The most common sources of bacteraemia were central venous catheter infection (117/296, 39.5%) and unknown primary site (97/296, 32.8%). Sixty-one episodes (20.6%) were community-acquired and 235 (79.4%) were nosocomial. Forty-three patients (14.5%) died. Pneumonia (RR 1.5, 95%CI 1.1–14.2), age<65 (RR 3.1, 95%CI 1.4–10.3), hospitalization in the intensive care unit (ICU) (RR 3.2, 95%CI 1.3–9.8), rapidly fatal disease (RR 4.9, 95%CI 3.1–12.6), and severe sepsis (RR 9.8, 95%CI 1.6–19.7) were independent predictors of death. Factors predicting the probability that an episode of nosocomial bacteraemia was due to NF included: rapidly fatal disease (RR 1.23, 95%CI 1.02–4.1), age<65 (RR 2.05, 95%CI 1.4–3), hospitalization in the ICU (RR 2.06, 95%CI 1.4–3, and pneumonia (RR 2.1, 95%CI 1.05–4.8).
Discussion: NF bacteraemia mainly affects patients with malignant haematological disease, with and without transplantation, and patients in the ICU. The most common known source is a central venous catheter, though many sources are unknown. Mortality is relatively low, and depends on the severity of the underlying disease.
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Introduction |
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Pseudomonas aeruginosa is the best known and most important pathogen with clinical significance among the glucose non-fermentative Gram-negative bacilli.1,2 Other members of the group include other pseudomonads, Acinetobacter spp, Stenotrophomonas maltophilia, Alcaligenes spp, Flavimonas oryzihabitans, and Sphingobacterium spp (Flavobacterium).3 These apparently heterogenous micro-organisms have common traits of clinical importance that justify their inclusion and study in a single group: most of them cause nosocomial infections that usually take place in hosts with severe underlying diseases, and are usually multi-drug-resistant.4,5 Serious infections due to this group of micro-organisms are currently being reported with increasing frequency elsewhere,6–20 and they may make a significant contribution to in-hospital mortality.
Since 1991, we have recorded a large number of bacteraemias due to non-fermentative Gram-negative bacilli. We have reported our clinical experience with P. aeruginosa bacteraemia elsewhere,21–23 and now focus on bacteraemias due to the remaining members of the non-fermentative group: Acinetobacter sp., Pseudomonas sp. other than P. aeruginosa, Stenotrophomonas maltophilia, and others (NF). The objectives were to evaluate the epidemiology, ecology, main clinical characteristics and risk factors behind the poor outcome of such patients. We have also evaluated the predictors of NF aetiology in cases of nosocomial bacteraemia.
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Methods |
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Patients and data collection
We analysed historical data from patients over 14 years old whose blood cultures grew non-fermentative Gram-negative bacilli other than P. aeruginosa (NF), prospectively studied over a 10-year period (1 January 1991 to 31 December 2000) at the Infectious Diseases Service of the Hospital Clinic de Barcelona (Catalonia, Spain), a 900-bed tertiary care University teaching hospital, and at the Hospital Universitari de Tarragona Joan XXIII (Catalonia, Spain), a 350-bed University teaching hospital. Both hospitals have followed a blood culture surveillance program since 1990. Briefly, one infectious disease specialist and one microbiologist review the charts of patients with positive blood cultures, and recommend antibiotic therapy, according to clinical context and the results of the Gram stain, organism identification and sensitivities. The patient is then followed until discharge or death. Data regarding the episode of bacteraemia are thus collected prospectively, and entered in a database designed specifically for the blood culture surveillance program.
Microbiology
Blood cultures were drawn at the request of the patient's physician. At least two sets of blood cultures were drawn, usually from an antebrachial vein. Blood cultures were processed between 1991 and 1997 by the BACTEC NR-730 system (Beckton-Dickinson Microbiology Systems), and maintained routinely for 7 days; and since 1998 by the BACTEC-9240 system (Beckton-Dickinson Microbiology Systems), with an incubation period of 5 days. Acinetobacter sp., Alcaligenes sp., Flavimonas oryzihabitans, Pseudomonas sp., S. maltophilia, and Comamonas sp., among others, were identified according to the criteria previously described.24 Antimicrobial susceptibility tests were performed by a microdilution method with a commercial plate (Sensititre). An isolate was defined as susceptible or resistant according to the criteria of the National Committee for Clinical Laboratory Standards.25
Definitions
For easy interpretation of the results, episodes were viewed as patients (one patient had a second episode several years later). NF bacteraemia was defined as a blood culture in which any NF grew. Patients with polymicrobial bacteraemia were included in the study. An episode of NF bacteraemia was thought to be nosocomial if it took place 
72 hours after admission and/or if the patient had been hospitalized within 2 weeks before the current admission,26 otherwise the bacteraemia was classified as community-acquired. The underlying diseases and/or conditions of the patients were diagnosed using criteria reported elsewhere,27 and classified as non-fatal, ultimately fatal, and rapidly fatal.28,29
Glucocorticosteroid therapy was considered notable if the patient had been taking at least 30 mg of prednisone daily for at least 2 weeks before the detection of bacteraemia.30 Fever was defined as an axillary temperature >38 °C.27 Severe sepsis was defined according to criteria previously reported.31 Patients with neutropenia were defined as those who had a granulocyte count <0.50x109/l.32 Septic metastases were defined in cases with microbiological evidence of NF infection occurring >48 h after the bacteraemia had developed. Definitions of the source of bacteraemia, such as pneumonia, urinary-tract infection, surgical-site infection, or another, were as described previously.21,33 Central venous catheter was considered to be the source of bacteraemia when: (i) >15 CFU/ml of the same micro-organism was recovered in the semiquantitative culture of the tip than in blood cultures; or (ii) in the absence of another source, there were inflammatory signs (local pain and erythema, either with or without suppuration) in the area of insertion of the catheter and the fever disappeared in the first 24 h after the catheter was removed.34 A localized infection was thought to be the source if it was present before or at the same time as the development of bacteraemia, and culture of the site showed growth of the micro-organism isolated in the blood. When no focal infection could be demonstrated, the source was categorized as unknown.
Patients were considered to have received previous antibiotic treatment if this took place in the week before the development of the bacteraemia, and if it was administered for at least 48 h. Antibiotic therapy was considered empirical if it was instituted before the results of the cultures and sensitivity were known, and definitive when it was instituted after the microbiological results were known. Antibiotic therapies were considered appropriate if they included at least one drug active in vitro against the micro-organism responsible for the infection, and if the dose and pattern of administration were considered appropriate in terms of the current medical standards. Patients who did not received antimicrobial drugs were considered to have inappropriate antibiotic therapy.
Patients were followed-up until discharge (a mean of 10 days) or death. When the non-fermentative bacteraemia was the main cause of death (pneumonia with respiratory failure, severe sepsis or septic shock), the mortality was defined as directly related. In patients in whom other factors may have contributed to death, the mortality was considered indirectly related. Throughout most of the statistical analyses, overall mortality (direct plus indirect) was used.
Statistical analysis
The descriptive analysis was performed by calculating the mean and standard deviation (SD) for continuous variables. For categorical variables, absolute and relative frequencies were calculated. For the univariate analysis, the comparison between groups was done using the 
2 test or Fisher's exact test. A relative risk of death was arbitrarily assigned to the lowest risk category within each variable studied. For multivariate analysis, a logistic regression model was performed to determine the independent effect of the different risk factors for death. The variables included were: age <65 years, rapidly fatal disease, pneumonia as a source of the bacteraemia, central venous catheter infection as a source of the bacteraemia, hospitalization in the ICU, and severe sepsis. A second model was constructed to determine the predictive factors for acquiring nosocomial NF bacteraemia. The categories for comparison were a random selection of the 50% of the nosocomial bacteraemias due to all other micro-organisms, the proportion of cases and controls being 1:3. In this model, the variables were: age <65 years, malignant haematological underlying disease, rapidly fatal disease, previous antibiotic therapy, pneumonia, hospitalization >15 days, and hospitalization in the ICU. The variables of the models were selected according to their degree of independent association in the models performed previously and their epidemiological and/or biological plausibility. The agreed level of significance was <0.05. Data were analysed using the SPSS (v. 6.1)35 and the BMDP (module LR)36 programs.
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Results |
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There were 296 episodes of NF bacteraemia. Almost 87% (257/296) were due to Acinetobacter sp., S. maltophilia and Pseudomonas sp. other than P. aeruginosa (Figure 1
). There were 123 episodes of bacteraemia due to Acinetobacter sp. (107 (87%) due to Acinetobacter baumannii) and 75 episodes of bacteraemia due to Pseudomonas sp. other than P. aeruginosa (18 P. putida, 17 P. cepacia, 12 P. fluorescens, 10 P. stutzeri, 8 P. picketti, 5 P. paucimobilis, 3 other). The bacteraemia was polymicrobial in 81 cases (27.4%), and the accompanying micro-organisms were: staphylococci 37 (29 coagulase-negative staphylococci and 8 S. aureus), enterococci 19, other Gram-negative bacilli 11, and others 14. The 296 episodes represent 0.87 episodes per 1000 discharges and 3% of the total number of bloodstream infections seen at both hospitals, and remained stable during the period of the study. One hundred and sixty-six patients (56.1%) were male and the mean age of the whole group was 50 (SD 17.3) years (range 16–91 years). The bacteraemia was community-acquired in 61 (20.6%) and nosocomial in the remaining 235 (79.4%). Nosocomial cases represented 0.47 episodes/1000 discharges, and were 5.7% of nosocomial bacteraemias and 12% of Gram-negative nosocomial bacteraemias. The mean hospital stay of the patients who developed nosocomial NF bacteraemia was 18.1 (SD15.4) days, and in 27% of these patients hospitalization was >15 days.
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Regarding invasive procedures, 178 subjects (60.1%) had a central venous line placed; fifty-six (18.9%) had had previous surgery, and 52 (17.6%) had a urinary catheter placed. All but 16 patients (94.6%) had fever, 28 (9.5%) presented with severe sepsis, and one (0.3%) developed septic metastases. Fifty patients (16.9%) had neutropenia, and 78 (26.4%) were receiving steroids. The underlying conditions, and their associated mortality, are given in Tables 1
and 2. One hundred and ninety-three (65.3%) had fatal diseases (177 (91.7%) eventually fatal and 16 (8.3%) rapidly fatal), whereas 103 (34.8%) had non-fatal diseases.
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The sources of the bacteraemia were: intravenous catheter in 117 patients (39.5%); pneumonia in 31 (10.5%); urinary tract infection in 16 (5.4%); and ‘other’ in 35 (11.8%). Of these last, the most common sources were surgical site infection (12), soft-tissue infections (9), and implantable devices (6). In the remaining 97 episodes (32.8%), no obvious source of bacteraemia was identified. In these patients the source of bacteraemia was classified as ‘unknown’. The catheter was removed from 70/117 patients with intravenous catheter-associated bacteraemia and in 61 of these, the culture of the device showed growth of the micro-organism isolated in the blood.
One hundred and eighty-one patients (61.1%) had received previous antibiotic therapy. Two-hundred and seventy-one (91.6%) had received empirical antibiotic therapy. This was later considered appropriate on the basis of the results for sensitivity in 231 subjects (78%). The percentage of suitability of empiric antibiotic therapy for the most commonly recovered micro-organisms was: Acinetobacter sp. 100%, Pseudomonas sp. 88%, and S. maltophilia 51% (RR 5.5, 95%CI 3.2–9.3 for the latter). Definitive antimicrobial treatment was possible in 289 subjects, and was considered suitable in 287 (97%).
Twenty-eight patients (9.5%) presented with severe sepsis. Overall mortality was 14.5% (43/296): 37 (12.5%) deaths were directly related and six (2%) were indirectly related but while the infection was still active. Univariate analysis of the risk factors for death is shown in Table 3. No differences in mortality were detected between patients who received inappropriate vs. appropriate empirical antibiotic therapy: 13.8% vs 14.7%, respectively, even after excluding the 117 patients with central venous catheter-associated bacteraemia (RR 1.27, 95%CI 0.3–4.1). In relation to definitive antibiotic therapy, the mortality of those who were treated appropriately was 11.8% (34/287) whereas all nine of the patients who did not receive suitable antibiotics died. Regarding micro-organisms, the mortality rate was 23.7% (14/59) for S. maltophilia, 14.6% (18/123) for Acinetobacter sp., 8.6% (6/70) for Pseudomonas sp., and 11.4% (5/44) for the others. Variables that were independently associated with an increased risk of death are shown in Table 4.
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We compared the clinical characteristics of patients who developed nosocomial NF bacteraemia vs. nosocomial bacteraemia due to all other micro-organisms, to evaluate the predictive factors (if any) that the bacteraemia was due to a NF. The independent predictive factors found are shown in Table 5
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Discussion |
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This report shows that episodes of NF bacteraemia are low-virulence infections that are often related to invasive devices, and are frequently associated with concomitant micro-organisms. Most patients have haematological malignancies or some other cause of immunosuppression. Direct attributable mortality is weak, and seems to depend on the severity of the underlying disease. Data regarding the influence of suitable antibiotic therapy on mortality are inconclusive, and should be interpreted with caution.
Reports elsewhere show that Acinetobacter sp., Pseudomonas sp. other than P. aeruginosa, and S. maltophilia are the most common NF isolated in bacteraemia.7,10,13,16 Such figures correlate well with those presented here. Reports of Acinetobacter sp. bacteraemia are increasing. There have been reports of many outbreaks of Acinetobacter sp. bacteraemia in the last 10 years, both endemic and epidemic infections6,37,38 and in a large multicentre European study, Acinetobacter sp. bacteraemias represented 3.6% of the total isolates.39 At the same time, severe infections due to Pseudomonas sp. are also increasing. In a report from the early 1990s,16 the rate of bacteraemia increased from 3 per 10 000 admittances in 1972 to 14 per 10 000 admittances in 1986. The bacteraemia was usually due to an IV catheter that consequently had to be removed. Interestingly, in this early report mortality was 17%, which was lower than in cases of bacteraemia due to other Gram-negative bacilli. These figures are similar to those in this paper (see below). The literature shows that S. maltophilia is also emerging as a nosocomial pathogen, and bacteraemias due to this micro-organism almost tripled between the early and the late 1980s.16,40,41 The results presented here therefore confirm those reported in the literature, indicating that NF have recently become an important cause of bloodstream infection. The micro-organisms most commonly recovered are Acinetobacter sp. (specially A. baumannii), Pseudomonas sp. other than P. aeruginosa, and S. maltophilia.
NF bacteraemia affected patients of both sexes equally and affected patients of all ages, although patients were predominantly older people (especially in community cases). The common underlying diseases or conditions were transplants, carcinoma and steroid treatment. Therefore, as reported previously, nosocomial NF bacteraemia is usually presented in patients with severe underlying diseases and malignancy, usually either haematological/solid organ or due to transplantation.11,12,37 On the other hand, community cases occurred mainly in patients with non-malignant underlying diseases such as diabetes mellitus, renal failure or HIV-1 infection. Only 14 patients (4.5%) had no underlying diseases.
Our results highlight the fact that NF bacteraemia is often a central venous catheter-related infection8,12,13 (bacteraemia was attributed to a central venous catheter infection in almost 40% of our patients). This was particularly true for patients who presented with nosocomial NF bacteraemia, as this source was thought to be responsible in almost half of the patients. This numbers are lower than in most other studies regarding hospital-acquired bacteraemia. The difference probably arises from our definition of IV-catheter-related infection, which was more restrictive than is sometimes used.
The clinical evolution of the patients reported was not particularly striking; only a small percentage of patients developed severe sepsis and mortality was relatively low. As with P. aeruginosa bacteraemia21 and bacteraemia due to other micro-organisms,40 the mortality rate of patients with central venous catheter-related infection was low. This contrasts with patients who suffered from pneumonia, who had a high incidence of severe sepsis and death. In addition, elderly patients, patients with a short life expectancy due to severe diseases and those in the ICU had the worst prognosis.
One of the striking features was that the outcome of the patients was not related to the suitability of empirical antimicrobial therapy, and this situation was maintained even after we excluded the subset of patients with central-venous-catheter-related infection. The only exception was bacteraemia due to S. maltophilia. Empirical antibiotics were usually inappropriate for this group of patients, who also had the worst prognosis, compared to the other micro-organisms. With respect to the influence definitive antibiotic therapy on the outcome, our results suggest a poor prognosis for those who did not receive suitable antibiotics, but with reservations. Although all patients who did not received appropriate definitive antibiotics died, there were only nine. This low number does not permit definitive conclusions. How correct antibiotic treatment affects outcome has been evaluated in other studies, the results of which are controversial.10,16,42 While some have suggested that inappropriate antimicrobial treatment is an independent factor predictor of death,42 other studies found that, of all the therapeutic measures, removing an infected intravenous catheter had a greater impact on the mortality rate than the administration of antibiotics.16 It appears that patients who die due to NF bacteraemia are those who are in a critical condition because of a severe underlying disease (usually a malignant condition that is often disseminated and unresponsive to treatment) or because of prolonged hospitalization for chronic diseases. In this situation NF bacteraemia may be considered the final event that leads terminally ill patients to die. The patient's clinical condition is so impaired that even with correct antibiotic therapy, some will die.
Finally, we have identified several factors for predicting whether an episode of nosocomial bacteraemia is due to NF: notably, patients hospitalized in the ICU who develop nosocomial pneumonia, and those with rapidly fatal disease. This issue is of interest, because the identification of one or more of these factors could help the clinician to identify patients at risk for developing NF bacteraemia.
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Acknowledgments |
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This study was supported in part by a grant from the Fundación Máximo Soriano Jiménez and the Fundación Biociencia. We would like to thank Dr Jordi Rello for his critical review of the manuscript.
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Notes |
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Address correspondence to Dr F. Vidal, Infectious Diseases Unit, Department of Internal Medicine, Hospital Universitari de Tarragona JOAN XXIII, Mallafré Guasch 4, 43007 Tarragona, Spain. e-mail: fvidal{at}comt.es
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