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Predictors and outcome associated with an Enterococcus positive isolate during intensive care unit admission.

Enterococci are Gram-positive bacterial commensals of the gastrointestinal and female genital tracts of humans. Enterococcus faecalis and E. faecium are usually considered organisms of relatively low virulence, although invasion can result in urinary tract infections, endocarditis, bacteraemia, meningitis and intra-abdominal infections (1). Enterococcus spp. are common nosocomial pathogens in the USA, responsible for three to four cases of nosocomial bloodstream infections per 10,000 hospital discharges (2), and the third most common cause of bloodstream infections reported in combined medical-surgical intensive care units (ICU) (3). Since the isolation of vancomycin-resistant enterococci (VRE) in Europe in 1987 (4), the organism has emerged as one of the most feared nosocomial pathogens. Recently published guidelines from the Infectious Diseases Society of America strongly advocate against empiric therapy directed at enterococci because of concerns about antimicrobial resistance (5).

Cefepime (FEP) and piperacillin-tazobactam (TZP) are commonly used alternatives for the [beta]-lactam component of broad-spectrum regimens for empiric treatment of sepsis in the critically ill. Concerns about the relative activity against Enterococcus spp. of FEP (minimal inhibitory concentration [MIC] = 4 to 12 mg/l), compared to TZP (MIC = 0.4 to 1.6 mg/l for piperacillin), carbapenems (MIC = 1 to 2 mg/l for imipenem), ampicillin (AMP) (MIC = 1 to 5 mg/l against E. faecalis, although E. faecium is commonly resistant) and vancomycin (MIC = 0.2 to 6 mg/l) (6) means that some clinicians routinely add anti-enterococcal cover to FEP therapy for suspected intra-abdominal sepsis. In this study, we analysed the incidence of enterococcal colonisation and/or infection and the risk factors for a positive enterococcal isolate and in-hospital mortality, with particular reference to empiric antibiotic therapy (7).



The data are derived from two large general medical and surgical ICUs at Royal Brisbane and Women's Hospital (RBWH) and Westmead Hospital (WH), which collaborated in an antibiotic cycling study in 2004 to 2005 with four month cycles of either TZP or FEP as the [beta]-lactam component of the empiric regimen for sepsis of unknown aetiology. AMP was included in the FEP cycle at RBWH, but not at WH. Cycling dates were as follows:

1. RBWH: TZP period for admissions from 9 August 1. to 8 December 2004 and from 9 April to 8 August 2005; FEP and AMP period for admissions from 9 December 2004 to 8 April 2005.

2. WH: FEP period for admissions from 5 April 2. to 8 August 2004 and from 6 December 2004 to 3 April 2005; TZP period for admissions from 9 August to 5 December 2004 and from 4 April to 31 July 2005.

RBWH is a 948-bed tertiary referral and public teaching hospital, with a 26-bed closed medical and surgical ICU that admits approximately 1700 adult patients each year with a mean Acute Physiology and Chronic Health Evaluation (APACHE) II score of 16.5 for all patients. WH is an 800-bed tertiary referral and university affiliated teaching hospital with 20 ICU beds, taking approximately 900 admissions per annum with a mean APACHE II score of 20.

Data collection and definitions

Information on baseline variables, including patient age, gender, severity of illness at ICU admission as determined by the APACHE II score (8) and admission type (medical or surgical) were prospectively recorded. Clinical variables included operative intervention (that is, surgery immediately prior to admission to the ICU or an operative procedure during their ICU stay), presence of a nasogastric tube, arterial line, central venous catheter, urinary catheter, intercostal drain and intracranial pressure monitor or having received renal replacement therapy during their ICU stay.

The incidence of a positive enterococcal isolate during admission to the ICU was calculated for admissions between 9 August 2004 and 8 August 2005 at RBWH and between 5 April 2004 and 31 July 2005 at WH. Uncomplicated admissions discharged to the ward within 48 hours were not included. Repeat isolates of the same species in a single patient were counted once and the incidence was expressed as the number of patients per 100 admissions (percent of admissions) included in the study.


Approval for this study was obtained from the Human Research Ethics Committee of both institutions.

Statistical analysis

The association of baseline and clinical characteristics with a positive enterococcal isolate during ICU admission was evaluated in bivariate analysis. A Pearson chi-square test or Fisher's exact test was used for categorical variables and an independent t-test was used for continuous variables. Mean and standard deviation (SD) are reported for normally distributed data; non-normal data were log-transformed prior to testing (geometric means reported). Independent risk factors for a positive enterococcal isolate during ICU admission were determined by multivariate logistic regression modelling. All variables with P <0.10 in bivariate analysis were entered into the multivariate model, with backward elimination (P >0.05) subsequently performed; odds ratios (OR) and 95% confidence intervals (CI) are reported. The association between antibiotic use in the first 48 hours of ICU admission, baseline characteristics and clinical variables with in-hospital mortality in all patients included from both hospitals and for the sub-group of patients with positive enterococcal isolates was similarly analysed using logistic regression. Statistical analysis was conducted using SPSS 15.0 (SPSS Inc., Chicago, Il, USA).


Study population and risk factors for a positive enterococcal isolate

Excluding uncomplicated postoperative admissions, a total of 1855 patients were admitted on 1956 occasions to the RBWH and WH ICUs during the study period. Sixty-seven separate admissions involving 66 patients (3.4% of all admissions) had Enterococcus spp. (mostly E. faecalis) isolated during their ICU stay (Table 1); 7.5% of isolates (5/66) were VRE. Blood isolates were most common (18 patients), followed by urine (12 patients), catheter tip (11 patients), swab (10 patients), fluid (10 patients), tissue (eight patients) and endotracheal aspirate or lavage specimens (five patients). Isolation of Enterococcus spp. were associated with greater age and higher APACHE II scores on ICU admission and with several other variables normally associated with a higher level of care and acuity of illness, including hospital length of stay and in-hospital mortality (Table 2). Independent risk factors remaining after multivariate analysis were: meropenem/imipenem use within 48 hours of ICU admission (OR = 5.7, 95% CI 2.4 to 14, P <0.001), presence of a nasogastric tube (OR = 4.1, 95% CI 1.3 to 14, P = 0.018), FEP use within 48 hours of ICU admission (OR = 2.5, 95% CI 1.2 to 5.3, P = 0.017), renal replacement therapy (OR = 2.2, 95% CI 1.0 to 4.7, P = 0.046), operative intervention (OR = 1.8, 95% CI 1.0 to 3.2, P = 0.035) and age (OR = 1.2 for each 10 year increase, 95% CI 1.1 to 1.5, P = 0.009).

Antibiotic usage by empiric antibiotic cycling period

Twenty-seven percent of patients (301/1134) received TZP during the period in which TZP was the protocol-specified antibiotic for empiric therapy of sepsis of unknown aetiology. Thirty-two percent of patients (263/822) received FEP during the period in which FEP was the protocol-specified empiric antibiotic. During the TZP period, 1.7% of patients (19/1134) received FEP, while 4.7% of patients (39/822) received TZP during the FEP period.

During the periods in which both RBWH and WH specified the use of FEP for empiric sepsis of unknown aetiology, 17% of RBWH patients (50/291) received AMP while at WH, where AMP was not routinely added to enhance enterococcal cover for suspected gastrointestinal-associated infection treated with FEP, 8.9% of patients (47/531) received AMP (P <0.001). There was no difference between the specified FEP and TZP periods in the use of meropenem/impenem (7.9% or 65/822 vs 8.1% or 92/1134, respectively; P = 0.87) or vancomycin (23% or 186/822 vs 21% or 236/1134, respectively; P = 0.34).

Incidence of enterococcal colonisation and infection

The incidence of ICU-identified enterococcal isolates was 4.2 per 100 admissions at RBWH (36/852) and 2.8 per 100 admissions (31/1104) at WH (P = 0.087) (Table 3). Rates of enterococcal isolates were similar during the FEP cycling period compared to the TZP cycling period (3.4 per 100 admissions vs 3.4 per 100 admissions, respectively; P = 0.97). The relative proportion of VRE isolates to total enterococcal isolates was 5.6% (2/36) in the RBWH sample and 9.7% (3/31) in the WH sample (P = 0.66), while overall rates were low (0.2% or 2/852 and 0.3% or 3/1104, respectively).

Mortality prediction in the whole sample

A logistic regression model predicting in-hospital death for the study sample as a whole identified the following factors: renal replacement therapy (OR = 2.3, 95% CI 1.4 to 3.6, P = 0.001), APACHE II score (OR = 1.7 for each five-point increment, 95% CI 1.5 to 1.8, P <0.001) and age (OR = 1.1 for each 10 year increase, 95% CI 1.0 to 1.2, P = 0.030). Surgical patients had a lower odds of death (OR = 0.70, 95% CI 0.52 to 0.95, P = 0.021). A positive enterococcal isolate was not an independent predictor of mortality (OR = 1.6, 95% CI 0.80 to 3.2, P = 0.18). Pre-emptive anti-enterococcal therapy (AMP, TZP, meropenem/imipenem or vancomycin) was significantly associated with mortality in bivariate analysis (OR = 1.5, 95% CI 1.1 to 2.0, P = 0.004), but was not independently predictive in multivariate analysis.

Predictors of mortality in patients with enterococcal isolates

In patients with a positive enterococcal isolate (n = 66), female gender, surgical admission, the presence of a nasogastric tube, arterial line insertion, renal replacement therapy and a higher APACHE II score were associated with hospital mortality with a P <0.10 in bivariate analysis. However, only renal replacement therapy was independently predictive of mortality in multivariate analysis (OR 6.2, 95% CI 1.4 to 27, P = 0.015). AMP (OR = 0.60, 95% CI 0.042 to 8.4, P = 0.70), FEP (OR = 3.6, 95% CI 0.62 to 21, P = 0.15), TZP (OR = 4.2, 95% CI 0.71 to 25, P = 0.17), meropenem/imipenem (OR = 0.16, 95% CI 0.012 to 2.2, P = 0.17) and vancomycin (OR = 0.45, 95% CI 0.062 to 3.3, P = 0.43) use within the first 48 hours of ICU admission were not associated with mortality with forced entry into the multivariate model; APACHE II score was significantly associated with mortality in this model (OR 1.9 for each five-point increase, 95% CI 1.2 to 3.3, P = 0.013).


The most significant finding in our study was the low incidence of positive Enterococcus spp. isolates in both ICUs (3.4 cases per 100 admissions), although we observed a greater proportion of VRE than in previously published Australian data9. This is in contrast to the ICU infection rates reported from hospitals in the USA, where Enterococcus is the most common pathogen in surgical-site infections3. Rates of enterococcal infection reported elsewhere have ranged from 1.0 cases per 100 admissions in a multicentre Spanish study (10), to 6.7 cases per 100 admissions in a single unit in Greece (11).

Rates of VRE colonisation in our study (7.5%) were lower than in centres in North America, which have seen a dramatic increase from 0.3% in 1989 to 7.9% in 1993 (12), 24.7% in 1999 (13) and 27.5% in 200214. The SENTRy program, a global network of hospitals tracking antimicrobial susceptibility of pathogens, has similarly reported substantial increases in the proportion of VRE amongst enterococcal bloodstream infections, particularly in North America (15). Vancomycin resistance in E. faecium was also significantly higher in our study (5/17 or 29%) compared to the 8.9% observed in the Pan-European Antimicrobial Resistance using local Surveillance study (16) and the Australian Group for Antimicrobial Resistance in 1995 and 1999 (0 and 0.3%, respectively) (9).

In our study population, risk factors for a positive enterococcal isolate were age, operative intervention, presence of a nasogastric tube, renal replacement therapy and meropenem/imipenem and FEP use within 48 hours of ICU admission. Age has been found to be a significant risk factor in our study, although a similar study by Sitges-Sera et al did not find age to be an independent factor for postoperative enterococcal infection (17-20). A number of studies, however, have found age to be a significant factor for acquisition of VRE (17-20), compared to vancomycin-sensitive Enterococcus. A positive enterococcal isolate was also found to be more common in patients receiving renal replacement therapy in our study, although similar observations are lacking in literature. Patients on renal replacement therapy have been identified as a population with increased risk of infection due to VRE (18,21) and the frequent use of vancomycin in these patients may be a likely contributing factor to the increased risk of VRE-infection within this population (4). Furthermore, renal replacement therapy may be a marker of disease severity.

Our data demonstrated that exposure to meropenem or imipenem within the first 48 hours of ICU admission was significantly associated with acquisition of a positive enterococcal isolate. Although these drugs have not been specifically linked to increased incidence of enterococcal infection, previous studies have identified prior exposure to agents with anaerobic activity as a risk factor for VRE (21-23). Early or pre-emptive meropenem/ imipenem use may also be a marker for severity of illness. In our study, use of FEP in the first 48 hours was also associated with a positive enterococcal isolate. Although antibiotics such as FEP which do not disrupt the anaerobic microflora have not be shown to promote VRE colonisation in mouse models (24), a recent study by Paterson et al found that 31.1% of patients treated with FEP had rectal colonisation with VRE (25).

The presence of a positive enterococcal isolate was associated with a higher overall crude mortality rate than in patients with no isolates positive for Enterococcus. The 26% crude mortality rate we observed in our study is comparable with previous studies of patients with enterococcal infection (23,26,27). Enterococcal peritonitis has been associated with increased mortality (20,28), although the independent association of positive enterococcal isolates with mortality was only evaluated in one of these studies (20,28). Our larger study, which included patients with Enterococcus isolated from a range of different sites, found no independent association between a positive enterococcal isolate and mortality after controlling for age and severity of illness.

In our study, renal replacement therapy in ICU was a strong predictor of mortality, not only in the whole sample, but also among patients with positive enterococcal isolates. Although a similar observation has been made by lautenbach et al (18), other studies have shown no association between renal replacement therapy and mortality (21,29). The association of age and higher APACHE II scores with increased mortality is well recognized (21,29-31).

While Enterococci are an increasingly important cause of nosocomial infections, their clinical significance has been the subject of a long-lasting and ongoing debate (7,32). Our findings suggest that empiric AMP therapy was not associated with a reduction in in-hospital mortality, despite the fact that the majority of enterococcal isolates were E. faecalis, which are typically ampicillin-susceptible. This finding has been supported by a number of clinical trials (5,31,33,34). In a review of six clinical trials examining the use of antibiotics without in vitro activity against Enterococci in the treatment of intra-abdominal infections, there were no cases of treatment failure, despite 20 to 30% of cultures growing Enterococci (35). However, Vergis et al have shown that in cases of monomicrobial enterococcal bacteraemia, effective enterococcal therapy within 48 hours independently predicted survival (30). Similar observations have been made by others (20,36).

Although this study included a large cohort with prospective data collection by trained data collectors, there were several limitations. First, the study was not powered to detect a difference in the rates of enterococcal positive isolates between the two study sites or between the different cycling periods. Second, while empiric antibiotic therapy use was influenced by the cycling period, there was no randomisation or blinding, and sicker patients may have been more likely to receive early antibiotic therapy with anti-enterococcal cover. The presence of some clinician variability in the use of antibiotics may have introduced bias. Third, we looked only at enterococcal isolates obtained during the period of ICU admission and not during the overall hospital stay, which may have underestimated the enterococcal colonisation rate in this group of patients. We were also unable to determine whether pre-ICU colonisation increased the odds of subsequent infection. The retrospective limitations of this study meant it was not possible to obtain more detailed information on admission diagnosis, type of surgery and clinician opinion as to whether a positive enterococcal isolate was considered evidence of infection as opposed to colonisation. Due to retrospective limitations, we also equated antibiotic use in the first 48 hours with empiric therapy. Therefore, our study was unable to consider empiric therapy due to undifferentiated sepsis subsequent to this period.


Enterococcal infections are becoming increasingly prevalent worldwide. This large study confirms a low incidence of enterococcal colonisation and infection in two Australian ICUs. A positive enterococcal isolate, while not independently associated with mortality, may be a marker of the underlying severity of illness. In our study, factors associated with increased risk of acquiring enterococcal isolates include age, operative intervention, presence of a nasogastric tube, renal replacement therapy and meropenem/imipenem and FEP use within the first 48 hours of ICU admission. None of these factors, except for the need for renal replacement therapy, was associated with increased mortality, supporting the recently published Infectious Diseases Society of America guidelines advocating against empiric therapy directed at Enterococci (5). The addition of AMP to FEP in empiric treatment of sepsis remains of unproven value although this negative finding must be evaluated against other higher powered studies.


The authors thank the ICU research teams at RBWH and WH for their contribution to the study. Dr J Dulhunty was supported by a grant from the RBWH Research Foundation (2007) and by a Queensland Health clinical research position (2008) during preparation of this manuscript. The Australian Antibiotic Cycling Group, which includes Drs J Iredell, J Lipman, J Gallagher, J Faoagali, M Woods, N George and S Partridge, is grateful to the Australian and New Zealand Intensive Care Foundation for grant support.

Accepted for publication on May 18, 2009.


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I. CHATTERJEE *, J. M. DULHUNTY ([dagger]), J. IREDELL ([dagger]), J. E. GALLAGHER ([section]), A. SUD **, M. WOODS ([dagger][dagger]), J. LIPMAN ([dagger][dagger])

Department of Intensive Care Medicine, Royal Brisbane and Womens Hospital, Brisbane, Queensland, Australia

Authors representing the Australian Antibiotic Cycling Group.

* M.B., B.S., M.D., F.N.B., F.J.F.I.C.M, Staff Specialist, Department of Intensive Care Medicine, Toowoomba Hospital, Toowoomba.

([dagger]) M.B., B.S., M.T.H., Ph.D., Research Fellow, Department of Intensive Care Medicine, Royal Brisbane and Women's Hospital and Burns, Trauma and Critical Care Research Centre, University of Queensland.

([double dagger]) M.B., B.S., Ph.D., F.R.A.C.P., F.R.C.P.A., Associate Professor, Centre for Infectious Diseases and Microbiology, University of Sydney and Westmead Hospital, Sydney, New South Wales.

([section]) M.B., B.Ch., F.J.F.I.C.M., Senior Staff Specialist, Intensive Care Unit, Westmead Hospital, Sydney, New South Wales.

** M.B., B.S, M.D., F.R.A.C.P., Staff Specialist, Medical Assessment Unit and Infectious Diseases, Nepean Hospital, New South Wales.

([dagger][dagger]) M.D., M.P.H., F.A.F.P.H.M., F.R.A.C.P., F.A.C.P., Associate Professor, University of Queensland and Senior Specialist, Infectious Diseases Unit, Royal Brisbane and Women's Hospital.

([double dagger][double dagger]) M.B., B.Ch., D.A. (S.A.), F.F.A. (S.A.), F.F.A. (Crit. Care) (S.A.), F.J.F.I.C.M., M.D., Professor and Head, Anaesthesiology and Critical Care, University of Queensland, Director, Department of Intensive Care Medicine, Royal Brisbane and Women's Hospital and Burns, Trauma and Critical Care Research Centre, University of Queensland.

Address for correspondence: Dr I. Chatterjee, Staff Specialist, Department of Intensive Care Medicine, Toowoomba Hospital, Pechey St, Toowoomba, Qld 4350. Email:
Enterococcus spp. isolated by hospital and patient

Species RBWH, n WH, n Total, n

E. faecalis 31 18 49
E. faecium 2 10 12
E. faecium (VRE) 2 3 5
Unidentified Enterococcus spp. 1 3 4
Total 36 30* 66

RBWH=Royal Brisbane and Women's Hospital, WH=Westmead
Hospital, VRE=vancomycin resistant enterococcus. Note: multiple
isolates of the same species in the same patient were counted once.

* Multiple organisms (E. faecalis and E. faecium; E. faecalis, E.
faecium and VRE) isolated in two patients during the same ICU
admission; one patient admitted twice.

Factors associated with a positive enterococcal isolate
in bivariate analysis

 Enterococcus isolate

Characteristic yes (n=67)

Baseline characteristics
 Age (mean [+ or -] SD)* 60.1 [+ or -] 15.1
 Gender, male * 41 (62.1)
 APACHE II score 21.9 [+ or -] 7.6
 (mean [+ or -] SD)
Clinical variables
 Surgical admission 37 (55.2)
 Medical admission 29 (43.3)
 Operative intervention 41 (61.2)
 Nasogastric tube 58 (86.6)
 Urinary catheter 61 (91.0)
 Arterial line 60 (89.6)
 Central venous catheter 61 (91.0)
 Intercostal drain 11 (16.4)
 Intracranial pressure monitor 6 (9.0)
 Renal replacement therapy 12 (19.0)
Empiric therapy
 TZP ([dagger]) 9 (13.4)
 FEP ([dagger]) 10 (14.9)
 AMP ([dagger]) 5 (7.5)
 Meropenem/imipenem ([dagger]) 10 (14.9)
 Vancomycin ([dagger]) 12 (17.9)
 ICU length of stay 10.2 [+ or -] 3.8
 (g-mean [+ or -] SD)
 Hospital length of stay 35.2 [+ or -] 3.0
 (g-mean [+ or -] SD) *
 In-hospital mortality * 17 (25.8)

Characteristic No (n=1889) P value

Baseline characteristics
 Age (mean [+ or -] SD)* 54.2 [+ or -] 19.7 0.017
 Gender, male * 1103 (61.7) 0.94
 APACHE II score 19.4 [+ or -] 8.6 0.018
 (mean [+ or -] SD)
Clinical variables
 Surgical admission 1033 (54.7) 0.93
 Medical admission 839 (44.4) 0.86
 Operative intervention 792 (41.9) 0.002
 Nasogastric tube 1397 (74.0) 0.020
 Urinary catheter 1599 (84.6) 0.15
 Arterial line 1556 (82.4) 0.13
 Central venous catheter 1344 (71.1) <0.001
 Intercostal drain 144 (7.6) 0.009
 Intracranial pressure monitor 121 (6.4) 0.41
 Renal replacement therapy 111 (5.9) <0.001
Empiric therapy
 TZP ([dagger]) 178 (9.4) 0.27
 FEP ([dagger]) 126 (6.7) 0.023
 AMP ([dagger]) 88 (4.7) 0.25
 Meropenem/imipenem ([dagger]) 50 (2.6) <0.001
 Vancomycin ([dagger]) 148 (7.8) 0.003
 ICU length of stay 2.8 [+ or -] 3.4 <0.001
 (g-mean [+ or -] SD)
 Hospital length of stay 13.6 [+ or -] 3.5 <0.001
 (g-mean [+ or -] SD) *
 In-hospital mortality * 250 (14.0) 0.007

Number of patients and percent (in parentheses) reported,
unless otherwise indicated. SD=standard deviation,
TZP=piperacillin-tazobactam, FEP=cefepime, AMP=ampicillin,
g-mean=geometric mean. * The denominator is the number of
patients rather than the number of admissions (i.e. 66
and 1855, respectively). ([dagger]) Empiric therapy within
48 hours of ICU admission.

Rates of positive Enterococcus isolates during period
of empiric antibiotic cycle
 Positive isolate,
Cycle Hospital Admissions, n n (%)

TZP RBWH 561 22 (3.9)
TZP WH 573 17 (3.0)
FEP + AMP RBWH 291 14 (4.8)
FEP WH 531 14 (2.6)

TZP=piperacillin-tazobactam, RBWH=Royal Brisbane and
Women's Hospital, WH=Westmead Hospital, FEP=cefepime,
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Author:Chatterjee, I.; Dulhunty, J.M.; Iredell, J.; Gallagher, J.E.; Sud, A.; Woods, M.; Lipman, J.
Publication:Anaesthesia and Intensive Care
Article Type:Report
Geographic Code:8AUST
Date:Nov 1, 2009
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