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Original Report Nosocomial Gram-Negative Bacteremia Geoffrey D.Taylor, MD;” Maureen Buchanan-Chell, Bs~N;~Terri Kirkland, BSCN;~ Margaret McKenzie, BScN;+ and Rhoda Wiens, BScNt ABSTRACT Objective: To review experience with hospital-acquired bacteremia due to aerobic gram-negative bacilli at the University of Alberta Hospital, episodes of nosocomial bacteremia occurring between August 1986 and June 1995 were analyzed. Methods: Since 1986, prospective surveillance has been conducted for the occurrence of hospital-acquired bloodstream infections. Cases were detected by monitoring positive blood culture results reported by the institution’s clinical microbiology laboratory. Following chart review, isolates were categorized as representing a hospital-acquired infection, a communityacquired infection, or contamination, based on Centers for Disease Control and Prevention criteria. Cases were followed for 1 week to determine outcome. Results: There were 584 episodes of gram-negative bacteremia, 28.9% of all hospital-acquired bloodstream infections. The gram-negative infection rate per 1000 admissions was unchanged from 1986 to 1995, but fell as a proportion of all infections from 37.9% in 1987 to 19.8% in 1995. Escherichia coli, Klebsiella spp, Pseudomonas spp, and Enterobacter spp were the most commonly identified species, accounting for more than 85% of episodes; only the incidence of Enterobacter changed, increasing from 2 per 10,000 admissions in 1987 to 5.2 per 10,000 in 1995. The 1 -week mortality rate gradually fell, from over 18% in 1987 to less than 5% in 1996 and averaged 14% for monomicrobial episodes. Pseudomonas infections were associated with significantly higher mortality (25.3%, relative risk 2.2) and Enterobacter infections with a significantly lower mortality (5.4%, relative risk 0.4). Conclusion: Over the past 9 years, the experience with the hospital-acquired bacteremia due to aerobic gram-negative bacilli at the University of Alberta Hospital revealed no significant change in the rate, causative organisms, organism-specific rates, or sources. However, as the incidence of infections due to other organisms has risen, the proportion of nosocomial * Department of Medicine, Unit, University of Alberta Received: November Address correspondence sity ofAlberta Hospital, 202 University Hospital, ofAlberta; Edmonton, 20,1996;Accepted:January and +Infection Alberta. Control 21,1997. to Dr. Geoffrey Taylor, 2E4.11 VM.C., Univer8440 112 Street, Edmonton,AB, CanadaTGG 2B7. bloodstream infections attributable isms has gradually fallen. Key Words: Int J Infect bacteremia, Dis 1997; to gram-negative gram-negative, organ- nosocomial 1:202-205. Nosocomial infections occur in 5 to 10% of hospitalized patients and have been identified as a significant public health problem. I>2Bacteremic nosocomial infections account for less than 5%, but result in greater attributable mortality, prolongation of length of hospitalization, and higher cost of care than other infections.1-3 Bacteremia due to gram-negative organisms has previously been recognized as an uncommon but often fatal complication of hospital care.4-8 Since 1986, blood culture reports have been prospectively monitored at University of Alberta Hospital to determine the incidence of nosocomial bloodstream infection. Studies of specific organ system infections resulting in bloodstream infection have been reported.9J0 The present study examines the incidence, sources, trends, and outcome of nosocomial bacteremia due to aerobic gramnegative bacilli. METHODS The University ofAlberta Hospital is a tertiary acute care facility and principal teaching hospital of the University of Alberta Faculty of Medicine. All forms of acute medical care were provided during the survey period, including adult and pediatric medicine and surgery, obstetrics-gynecology, oncology, and solid organ transplantation.The hospital has seven intensive care units (ICUs) for critically ill patients: cardiac, adult medical surgical, cardiac surgery, burns, neurosurgery, pediatric, and neonatal. In 1986, at the beginning of the survey, there were approximately 1100 inpatient bedsThrough the study period there was a gradual reduction in bed numbers reaching 560 in 1995, an approximate 50% overall reduction; however, annual patient admissions have been unchanged, averaging 30,500 per year; average length of stay has decreased and patient severity of illness and complexity has increased. Nosocomial Other than in ICUs, where phlebotomy was performed by registered nurses, blood cultures were obtained by physicians. Blood cultures were typically performed in sets of two and incubated aerobically and anaerobically for 7 days (unless prolonged incubation was requested), using the Bactec 9240 system (Becton and Dickenson Diagnostic Instrument Systems, Sparks, MD). Blood cultures reported as growing microorganisms were reviewed daily by nurse practitioners in the hospital’s infection control program. Patient charts were reviewed.The isolate was classified as a contaminant or resulting from a community-acquired or nosocomial infection based on Centers for Disease Control and Prevention (CDC) criteria.‘l The source of infection was determined by chart review. Service or ward where the patient was located when signs or symptoms of infection first developed was recorded.The patient was followed for 1 week from first positive blood culture to determine short-term outcome. Cases were reviewed by a physician (GT) prior to inclusion in the data-base. The data-base was reviewed for cases of gram-negative bacteremia occurring between August 1,1986, the initiation of the surveillance program, and June 30,1995.A case was included in the study if an aerobic gram-negative bacillus had been identified in the blood culture, either alone or as part of a polymicrobial infection. RESULTS There were 584 episodes of nosocomial gram-negative bacteremia in the 107 months of study (494 monomicrobial and 90 polymicrobial), representing 28.9% of all nosocomial bloodstream infections. Whereas the incidence of nosocomial bloodstream infection from all causes gradually increased through the study period, the rate for gram-negative infections was unchanged, averaging 2. I6 per 1000 admissions, so that the proportion of infections due to gram-negative bacteria fell from 37.9% / Table 30, infection 1995. in Univer- Nosocomial 1. / TuyZor et al Bacteremia Gram-Negative Organisms Bacteremia*: Number n = 610 (%) E. coli Klebsiella spp Pseudomonas spp Enterobacter spp Serratia spp Proteus mirabilis Acinetobacter spp Citrobacter spp Stenotrophomonas Other species+ 208 130 94 92 31 14 10 IO 8 13 *Monomicrobial Aeromonas malfophilia and polymicrobial (Z), Burkholderia cases: +Morganel/a cepacia (l), Alcaiigenes 203 Identified Organism (34.3) (21.5) (15.5) (14.5) (5.1) (2.3) (1.6) (1.6) (1.3) (2.2) (5), Providencia (Z), (I), Pasteurella (1). in 1987, the first complete year of the survey, to 19.8% in the first 6 months of 1995 (Figure 1). There were 610 aerobic gram-negative bacilli identified in the 584 episodes (Table 1). Escberichia coli (34.3%), Klebsiella species (21.5%), Pseudomonas spp (15.5%), and Enterobacter spp (14.5%) were most common, accounting for more than 85% of all episodes. No change occurred in annual incidence of any bacterial species, except for an increase in infections due to Enterobacter spp, (from 2.0/10,000 admissions in 1987 to 5.2/10,000 in 1995), which was not statistically significant (P > 0.05 by &i-square for trend). Table 2 demonstrates the source of infection for episodes of gram-negative bacteremia; urinary tract was most common (27.4%), followed by primary infection (i.e., those for which no underlying source could be identified) (24.8%), gastrointestinal source (17.2%), and lower respiratory tract (15.7%).The most common source of E. coli was the urinary tract (43%), followed by the gastrointestinal tract (21%); the respiratory tract was a rare source of E. coli (8%). Klebsiella and Enterobacter infections were most often attributed to a primary source (33.8% and 38.6%, respectively), followed by a urinary tract source (16.9% and 19.3%). Pseudomonas infections were most commonly attributed to a lower respiratory tract infection (3 1.9%), followed by primary infection (21.3%), and were rarely due to a gastrointestinal source Table Figure 1. Incidence of nosocomial bloodstream sity of Alberta Hospital, August 1, 1986 to June Gram-Negative 2. Nosocomial Gram-Negative Bacteremia Sources Source Number n = 584 (%) Urinary tract Primary* Gastrointestinal tract Lower respiratory tract Surgical site Skin (including burn) Other 160 145 101 92 39 34 13 (27.4) (24.8) (17.2) (15.7) (6.7) (5.9) (2.2) *Defined as a case of bloodstream infection that, following review, cannot attributed to an infection al another body site. be 204 International Journal Figure 2. Rate of mortality ture verifying gram-negative trend). of Infectious Diseases / Volume 1, Number 4, April 1997 within 1 week of first positive blood culbacteremia (P = 0.028 by x2 for linear (7%). No changes in relative frequency of overall sources of infection or organism-speciftc sources occurred during the 9 study years. Of the 494 monomicrobial episodes, 68 (13.8%) were associated with death within 1 week of first positive blood culture. The l-week mortality rate gradually fell through the study period from 18.3% in 1987 to 4.8% in the first 6 months of 1995 (p = 0.028 by chi-square for linear trend) (Figure 2). Mortality for monomicrobial Pseudomonas cases was 25.3% (28/86) (P < 0.01; relative risk, [RR] 1.81; 95% confidence interval [CI], 1.15-2.85) and for Enterobacter cases was 5.4% (5/80) (P = 0.05; RR, 0.41; 95% CI, 0.07-0.99). DISCUSSION Despite changes in health care delivery at the University of Alberta Hospital, including major reductions in bed numbers, shortened length of stay, and increased patient acuity resulting in increased susceptibility to infection, the epidemiology of nosocomial bloodstream infections due to gram-negative bacteria has remained remarkably constant within the institution. Over the past 9 years there has been no significant change in the rate, causative organisms, organism-specific rates, or sources of gram-negative sepsisAs there has been no significant change in annual blood culture numbers or laboratory methodology there should be no diagnostic artefact influencing the trend. One possible explanation for the lack of change in incidence of gram-negative bacteremia is that prevention techniques have kept pace with increasing patient susceptibility. However, no particular prevention intervention can be identified that would have had widespread impact on the incidence of gram-negative infections. Four organisms, namely E. coli, Klebsiella, Pseudomonas, and Enterobacter accounted for the majority of episodes; all other gram-negative bacilli together accounted for less than 15%. As the incidence of infections due to other organisms, particularly gram-positive cocci, has risen, the proportion of nosocomial bloodstream infections attributable to gram-negatives has gradually fallen, so that by the first half of 1995 less than 20% were associated with gram-negative bacteria, compared to 37.9% in 1987, the first full year of the study. The rise in incidence of gram-positive infections has been documented elsewhere and has been attributed to increased use of intravascular catheters of various types.4,5,‘2 The originating sources of infection for episodes of nosocomial gram-negative sepsis in the present study generally were not unexpected.The prominence of the urinary tract as a source represents a potential opportunity to reduce the incidence of nosocomial gram-negative sepsis. Since a large majority of bacteremic nosocomial urinary tract infections are a consequence of urinary catheter use, and since studies from other institutions have shown a high rate of inappropriate use of catheters, reducing inappropriate catheter use could potentially reduce the rate of nosocomial gram-negative sepsis.13x14 Some of the 24.8% of cases that were considered “primary” may have been attributable to vascular catheters, but it seems likely many were not. It is surprising that in so many cases of gram-negative sepsis neither the authors nor the clinicians providing care for the patient could determine the source of infection. A l-week follow-up period was chosen in part for surveillance convenience and in part to estimate the immediate mortality Impact of septicemia.The overall lweek mortality rate of 13.9% for monomicrobial cases cannot be considered an attributable mortality, since many of these patients had other significant medical problems, but can provide an estimate of the short-term impact of gram-negative septicemia. The much higher mortality associated with Pseudomonas sepsis was not unexpected, as this organism previously has been associated with a high mortality risk6-8;however, the trend to a lower mortality risk with Enterobacter sepsis was unexpected and should be confirmed by further studies. The downward trend in l-week mortality was steady, from 18.3% in 1987 to 4.8% in the first half of 1995, but whether this reflects a similar reduction in hospital mortality or attributable mortality is uncertain and would need to be determined by further studies.As there was no change in source or organism causing gram-negative sepsis, some other factor or factors must account for this downward trend. Supportive therapy and specific antimicrobial therapy has gradually been modified over the past decade, but no single intervention has been shown to dramatically improve the outcome of patients experiencing gram-negative sepsis. 15,16 This would be consistent with a steady decline in mortality rather than a dramatic Nosocomial reduction vention. at one point in time owing to a single inter- REFERENCES 1. Haley RW, Culver DH,White JW Morgan WM, Emori TG.The nationwide nosocomial infection rate.A need for a new vital statistic.Am J Epidemiol 1985; 121:159-167. 2. Public health focus. 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