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J Am Soc Nephrol 15:454-462, 2004
© 2004 American Society of Nephrology

CLINICAL SCIENCE

Effect of Nosocomial Bloodstream Infection on the Outcome of Critically Ill Patients with Acute Renal Failure Treated with Renal Replacement Therapy

Eric A. J. Hoste*, Stijn I. Blot*, Norbert H. Lameire{dagger}, Raymond C. Vanholder{dagger}, Dirk De Bacquer§ and Francis A. Colardyn*

*Intensive Care Unit, {dagger}Renal Division, and §Department of Public Health, Ghent University Hospital, Gent, Belgium.

Correspondence to Dr. Eric Hoste, Intensive Care Unit, 2K12-C, Ghent University Hospital, De Pintelaan 185, 9000 Gent, Belgium. Phone: 32-9-240-27-75; Fax: 32-9-240-49-95; E-mail: erik.hoste{at}UGent.be


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 References
 
ABSTRACT. Critically ill patients with acute renal failure (ARF) treated with renal replacement therapy (RRT) have a high mortality. The authors evaluated a cohort of 704 consecutive intensive care unit (ICU) patients with ARF treated with RRT to determine whether there was an increased incidence of nosocomial bloodstream infection and whether this resulted in a worse outcome. The incidence of nosocomial bloodstream infection was 8.8%, higher than that reported in other series of general ICU patients and also higher than the 3.5% incidence of bloodstream infection in non-ARF patients in the same unit (P < 0.001). There were more bloodstream infections caused by Gram-positive species compared with Gram-negative species or fungi. The distribution over the species was comparable to that reported by others for a general ICU population. The outcome was evaluated with matched cohort analysis. With this technique, patients with bloodstream infection (exposed) were closely matched with patients without bloodstream infection (non-exposed) in a 1:2 ratio. Matching was based on the APACHE II system and length of stay before bloodstream infection (exposure time). Length of stay and mortality were equal in exposed and non-exposed patients. There was also no difference in hospital costs. It can be concluded that critically ill patients with ARF treated with RRT were more susceptible to nosocomial bloodstream infection. Nevertheless, the outcome was not influenced by the presence of bloodstream infection. The high mortality observed in ARF patients could therefore not be attributed to the higher incidence of bloodstream infection.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusions
 References
 
Patients with acute renal failure (ARF) and need for renal replacement therapy (RRT) are among the sickest of the critically ill; their mortality, reported in recent trials, varies between 38 and 82% (1–8). Nosocomial bloodstream infection might be a contributing factor for the high mortality in this patient population.

There are to the best of our knowledge no data on the incidence of nosocomial bloodstream infection in ARF patients who are treated with RRT or on the effect of nosocomial bloodstream infection on outcome in this subset of patients.

Critical illness predisposes to colonization and infection with typical hospital bacteria like Enterobacter species, Serratia species, Pseudomonas species, Candida species, Coagulase-negative staphylococci, and methicillin-resistant Staphylococcus aureus (9). Contributing factors are the longer length of stay, exposure to invasive therapies and catheters, and reduced immunity (10). ARF patients have additional risk factors for bloodstream infection, as they are instrumented with extra intravenous catheters necessary for vascular access for RRT. This catheter is manipulated at the beginning and end of each RRT session and carries a high risk for colonization. In addition, there is evidence that patients with renal failure also have a decreased immunity (11, 12), promoting infection in general and/or colonization of the catheter, clinical situations that are at the origin of bloodstream infection. It has already been shown that patients with chronic, end-stage renal disease experience attributable mortality in case of nosocomial bloodstream infection (13). Although the literature is less prolific on the subject of immunity in patients with ARF, there is evidence that patients with ARF suffer from decreased immunity as well (14).

The aim of this study was to evaluate the epidemiology of bloodstream infection in a cohort of critically ill patients with ARF who were treated with RRT. In addition, it was analyzed whether this condition caused extra mortality and prolonged the length of stay in the hospital.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusions
 References
 
Setting
The study was conducted in the intensive care unit (ICU) of the Ghent University Hospital, a tertiary referral center with 1060 beds. The ICU has 54 beds and includes a medical, surgical, burns, and cardiac-surgical unit.

Patient Management
RRT was instituted in patients with ARF fulfilling at least one of the following criteria: blood urea >200 mg/dl, fluid overload and oligo-anuria (<400 ml/d), serum bicarbonate <15 mEq/L, or serum potassium >6.0 mmol/L (8,15). Continuous modalities of RRT, either CVVH or CVVHDF, were used in patients with severe hemodynamic instability (high dose of vasoactive therapy needed). Intermittent RRT was performed on a daily basis in the remaining patients. The indication for RRT, and choice of modality of RRT, was independently made by the attending renal consultant who was not involved in the present analysis.

Microbiological monitoring of patients, and assessment of colonization status, was performed by thrice-weekly sampling of oral swabs, urine, and sputum when patients were on mechanical ventilation; additionally, anal swabs were sampled once weekly.

Hemocultures were taken on a routine basis when infection was clinically suspected or when a patient’s temperature rose above 38.4°C. In this way, only clinically significant nosocomial bloodstream episodes were included. Hemocultures were executed by following the BacT/Alert procedure (Organon Technika Corp, Durnham, NC), and a 10-ml blood inoculum was considered standard.

Data Collection
The study was performed on a cohort of all ICU patients with ARF who were treated with RRT during the between January 1, 1995, and December 31, 2000. This period was chosen on the one hand to evaluate a sample size as large as possible and on the other hand by the desire to evaluate a cohort of patients in which therapeutic options were relatively homogeneous. Patients were excluded from analysis when RRT was initiated before ICU admission, or for indications other than ARF (e.g., intoxication).

The data analyzed in the study were all collected prospectively. All microbiologically documented nosocomial bloodstream infections were prospectively screened by the center for infection control. This hospital-wide surveillance program was used to perform a retrospective search for all ICU patients with nosocomial bloodstream infection. Bloodstream infection was considered to be nosocomial when it was diagnosed at least 48 h after hospital admission. Only bloodstream infections acquired during RRT were taken into account. The source of the bloodstream infection was determined by intensive care physicians and microbiologists on the basis of isolation of the microorganism from the presumed portal of entry and clinical evaluation. Antimicrobial resistance (AM-R) or susceptibility (AM-S) was determined according to methods for disk-diffusion testing by the National Committee for Clinical Laboratory Standards (16). AM-R was defined as in vitro resistance to ceftazidime for Gram-negative bacteria. In our hospital, ceftazidime is considered to be an indicator of epidemic extended-spectrum {beta}-lactamase-producing strains or hyperproducers of {beta}-lactamases; therefore, it is a sign of infection with organisms that are resistant to multiple drugs (17,18).

Because susceptibility patterns for Pseudomonas aeruginosa vary, these isolates were considered AM-R when there was resistance to one of the following antipseudomonal antibiotics: ceftazidime, imipenem, ciprofloxacin, or piperacillin (17,19). Staphylococci were defined as AM-R when there was resistance for methicillin; other Gram-positive bacteria were defined as AM-R in case of glycopeptide resistance. When there was resistance against fluconazole, Candida species were defined AM-R. During the study period, there was no change in microbiological laboratory technique.

Antimicrobial therapy was considered appropriate when the drugs used had an in vitro activity against the isolated strain, and inappropriate when not or if the patient did not receive antimicrobial treatment. The delay in the initiation of appropriate antimicrobial treatment was calculated from the day of onset of bloodstream infection.

Need for vasoactive therapy was defined as any dose of norepinephrine, epinephrine, vasopressin, dobutamine, and milrinone. Dopamine was also considered as vasoactive therapy when administered in a dose greater than 5 µg/kg per min.

Total cost of hospital stay was evaluated on basis of the hospital bill as it is stored in the computerized hospital administration system. As data from this system were not available for patients admitted in the year 1995, only patients admitted after December 31, 1995, were included in the cost analysis.

Study Design
Patient characteristics, comorbidity, and outcome were compared between patients with nosocomial bloodstream infection and those without in the whole cohort of patients with ARF who were treated with RRT. Also, renal impairment, defined by the Acute Dialysis Quality Initiative as either Loss of Kidney Function or End-Stage Kidney Disease (need for RRT for more than 4 wk or 3 mo, respectively) was compared between both groups (http://www.adqi.net/).

Furthermore, patients who survived were compared with patients who did not.

Matched Cohort Analysis
In this study design, ARF patients treated with RRT with nosocomial bloodstream infection during RRT were defined as exposed patients. We aimed to match every exposed patient with two other ICU patients with ARF who were treated with RRT but without clinical or microbiological evidence of bloodstream infection during RRT (non-exposed patients), although a match with one non-exposed patient was also accepted. The exposed:non-exposed ratio was aimed at 1:2 to reduce the risk of selection bias. Non-exposed patients were selected from the same period, and the selection was obtained without knowledge of outcome. Matching was based on length of ICU stay and the APACHE II classification system (20). Non-exposed patients had to have a length of ICU stay at least equal to the time it took for the corresponding exposed patient to develop bloodstream infection from ICU admission on. Exposure time was in other words equal for both exposed and non-exposed patients. Additionally, the patients had an equal principal ICU admission diagnosis according to the APACHE II classification and an APACHE II score that was maximally five points different from the case. The APACHE II score was calculated on basis of a chronic health evaluation and a set of acute physiologic parameters obtained during the first 24 h of ICU observation.

The APACHE II–predicted hospital mortality can be calculated with the APACHE II score and a factor attributed to each specific diagnostic category (surgical versus nonsurgical, elective or urgent surgery, major vital organ system failure, and the principle diagnosis leading to ICU admission). As predicted mortality can be derived from the APACHE II system, this matching procedure resulted in an equal predicted mortality for both exposed and non-exposed patients. This severity of disease scoring system has been used repeatedly in matched cohort studies dealing with nosocomial infections in the ICU setting (17,18,21–28).

When there were more than two corresponding non-exposed patients for an exposed patient, the non-exposed patients were matched on age, gender, and the nearest admission date.

Statistical Analyses
Data are expressed as mean ± SD and median (interquartile range). Univariate analysis of continuous variables was performed with the Mann-Whitney U test. The {chi}2 test was used for comparison of non-continuous variables.

Mortality attributable to bloodstream infection was determined in the matched cohort population by subtracting the crude mortality of the non-exposed patients from the crude mortality of the exposed patients (29). The crude relative risk (RR) was calculated as hospital mortality exposed/non-exposed, and the Mantel-Haenszel statistic was used to correct this crude mortality for the matched cohort design. Survival curves were prepared by means of the Kaplan-Meier method, and survival distributions were compared with the log-rank test. Finally, a Cox proportional hazards regression analysis was performed on the matched cohort of RRT patients to analyze whether there was an association of bloodstream infection with hospital mortality. To correct for the differences in severity of disease in patients, the following covariates were included in the model: age, gender, mechanical ventilation, and need for vasoactive therapy.

Significance was accepted for a two-sided P < 0.05. The statistical software packages SPSS 11.0.1 (SPSS Inc. Chicago, IL), Statistica, release 4.5 (StatSoft, Inc., Tulsa, OK), and SAS system, release 6.12 (SAS Institute Inc., Cary, NC) were used.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusions
 References
 
During the 5-yr study period, 704 patients with ARF were treated with RRT. In 62 patients (8.8%), a nosocomial bloodstream infection was documented. In six patients, two microorganisms were identified; therefore, a total of 68 microorganisms were documented in 62 patients. Bloodstream infection was documented 17 ± 15.0 d (14 [5.5 to 25.0]) after ICU admission and 13 ± 14.3 d (9 [2.0 to 21.3]) after initiation of RRT.

During the 5-yr study period, the sum of all lengths of duration of RRT was 11580 d; there were therefore 5.4 bloodstream infections per 1000 d of RRT.

The lungs were the most important source of bloodstream infection (26%), followed by the abdomen (23%), catheters for vascular access (16%), urogenital tract (10%), and wounds (6%). In 19% of the episodes of bloodstream infection, no source could be identified.

There were more bloodstream infections with Gram-positive bacteria compared with Gram-negative bacteria (Table 1); Gram-positive cultures had more AM-R (P < 0.001); this could mainly be attributed to methicillin resistance in coagulase-negative staphylococci. Detailed information concerning microbiological species involved and AM-R is illustrated in Table 1.


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  		Table 1. Micro-organisms involved in bloodstream infection in intensive care unit (ICU) patients with acute renal failure who were treated with renal replacement therapy
 
Antimicrobial therapy was adequate in 52 patients (83.9%); and delay in therapy in these patients was 0.4 ± 1 d (0 [0 to 0]). Colonization with the microorganism that caused the bloodstream infection was already present in 34 patients (54.8%).

Patients with nosocomial bloodstream infection were younger and were more severely ill as illustrated by the higher need for vasoactive therapy, mechanical ventilation, and length of mechanical ventilation (Table 2). More patients with bloodstream infection needed initiation of mechanical ventilation compared with patients without; there was no difference in mechanical ventilation before RRT. APACHE II score and predicted mortality were also higher in patients with nosocomial bloodstream infection, although these differences did not reach statistical significance (Table 2).


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  		Table 2. Patients with acute renal failure treated with renal replacement therapy. Comparison of patients without and with bloodstream infection (BSI). Data are illustrated as %, or mean ± standard deviation and median (interquartile range)a
 
Patients with nosocomial bloodstream infection were treated with RRT during a longer period of time; also more patients had loss of kidney function or end-stage kidney disease (need for RRT for more than 4 wk or 3 mo, respectively). Furthermore, length of stay in the ICU and hospital was longer for patients with bloodstream infection (median, 41 d extra or 78 d extra, respectively; both P < 0.001). Crude mortality was the same in patients with and without bloodstream infection (Table 2). This is also illustrated by the Kaplan-Meier survival plots for both groups (Figure 1). Although there was no difference in crude hospital mortality, the course of both survival curves was different (log-rank test, P = 0.004), with a better survival early during hospitalization for patients with bloodstream infection.



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  		Figure 1. Cohort analysis of all patients with acute renal failure (ARF) treated with renal replacement therapy (RRT). Kaplan-Meier survival curve for patients without bloodstream infection (non-exposed patients) (solid line) and with bloodstream infection (exposed patients) (interrupted line). Censored data are indicated with +.

 
Mortality in patients with a bloodstream infection with a Gram-positive microorganism was not different from that in patients with a Gram-negative species, a Candida species, or when two microorganisms were documented (67.9%, 72.7%, 66.7%, and 66.7%, respectively). Mortality in patients with resistant microorganisms was also equal compared with nonresistant species (63.9% versus 76.9%, P = 0.272). There was, however, a higher mortality in patients who had a bloodstream infection secondary to an infection, compared with those with a primary bloodstream infection (infected catheter or no source detected) (82.1% versus 47.8%, P = 0.005).

Patients who died had a higher APACHE II score and predicted mortality (Table 3). Furthermore, there was more associated organ failure as evidenced by more need for vasoactive therapy and mechanical ventilation. A greater proportion of non-survivors had initiation of RRT with CRRT. There was no difference in the proportion of patients with bloodstream infection in hospital survivors and non-survivors.


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  		Table 3. Patients with acute renal failure treated with renal replacement therapy. Comparison of patients who survived and patients who did not survive in hospital. Data are illustrated as %, or mean ± standard deviation and median (interquartile range)a
 
Matched-Cohort Analysis
For 56 patients (90.3%) with bloodstream infection, at least one non-exposed patient with ARF treated with RRT was found; for 50 patients, two non-exposed patients could be matched.

Non-exposed patients were well matched to exposed patients for age, gender, APACHE II, score and need for vasoactive therapy and mechanical ventilation (Table 4).


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  		Table 4. Matched cohort analysis. Comparison of patients with bloodstream infection (exposed patients) to patients without bloodstream infection (non-exposed patients). Data are illustrated as %, or mean ± standard deviation and median (interquartile range)a
 
More patients with bloodstream infection fulfilled the loss and end-stage kidney disease criteria as proposed by the Acute Dialysis Quality Initiative.

There was no significant difference in length of stay in the ICU or in hospital. Hospital mortality was slightly but not significantly higher for ARF patients with bloodstream infection compared with non-exposed patients (Table 4); this is also illustrated in the corresponding survival curves (log rank, P = 0.539) (Figure 2).



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  		Figure 2. Matched cohort analysis: Kaplan-Meier survival curve for patients without bloodstream infection (non-exposed patients) (solid line) and with bloodstream infection (exposed patients) (interrupted line). Censored data (mortality) are indicated with +. Length of stay: exposed patients, the length of hospital stay after bloodstream infection; non-exposed patients, length of hospital stay minus the length of ICU stay before bloodstream infection of the respective case patient.

 
The total hospital cost was higher for the exposed patients; however, this difference was not significant (Table 5).


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  		Table 5. Matched cohort analysis. Total hospital costs for patients with bloodstream infection (exposed patients) and patients without (non-exposed patients). Only patients admitted after December 31, 1995, were included in this analysis (n = 134). Data are illustrated as mean ± standard deviation and median (interquartile range)
 
The attributable hospital mortality for ARF patients with bloodstream infection was 6.4% (95% confidence interval [CI], -8.8% to 21.4%), as mortality rates for exposed and non-exposed patients were 69.3% and 63.2%, respectively (P = 0.413). The matched RR (corrected according to the Cochran-Mantel-Haenszel statistic was 1.09 (95% CI, 0.86 to 1.38; P = 0.46).

Cox multivariable analysis could identify an independent association between older age and mortality. There was however, no association between bloodstream infection and mortality in the unadjusted or in the covariate-adjusted analysis (Table 6).


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  		Table 6. Matched cohort analysis. Cox proportional hazards regression analysis unadjusted, and adjusted for age, gender, and need for mechanical ventilation and vasoactive therapya
 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusions
 References
 
We found that there was a high incidence of nosocomial bloodstream infection in a subgroup of severely ill patients with ARF who were treated with RRT in the ICU. Nosocomial bloodstream infection did not lead to a statistically significant increased length of stay, costs, or mortality. Therefore, these data do not support the hypothesis that the high mortality rate observed in ARF patients can be attributed to nosocomial bloodstream infection.

The incidence of nosocomial bloodstream infection in this group of ICU patients with RRT was higher than that of ICU patients without RRT in our unit (8.8% versus 3.5%, P < 0.001, unpublished data). Incidences of nosocomial bloodstream infections in ICU patients reported in the literature are invariably less than 5% (27,30–34). The high incidence of bloodstream infection in this study is therefore in support with the hypothesis that critically ill patients with ARF have a decreased immunity and are therefore more vulnerable to infections.

Whether the increased vulnerability for bloodstream infections could be attributed to uremia in this particular subgroup of patients remains an open question. It might therefore be interesting to evaluate whether different RRT options, such as continuous RRT versus intermittent RRT versus slow extended dialysis, or different doses of RRT, or early versus late initiation of RRT affect the incidence or severity of bloodstream infection.

The distribution of pathogens was comparable to that reported by Edmond et al. (9) in their 3-yr analysis of nosocomial bloodstream infections in 49 hospitals in the United States. The increased incidence could not be attributed to an isolated increase in infection rate of Gram-positives, Gram-negatives, or fungi. Hence, patients treated with RRT are not more prone to opportunistic pathogens like Pseudomonas aeruginosa or Candida species compared with a general population of critically ill patients, as could have been assumed on basis of their immune status. Therefore, these results could indicate that it was not the decreased immunity associated with ARF that caused the higher incidence of bloodstream infection, but rather the severity of illness of the patients.

There was an increased length of stay for the patients with nosocomial bloodstream infection in the whole cohort of patients. Hospital mortality was not different between patients with and without bloodstream infection. The increased length of stay was however confounded by the high mortality in the initial phase of ICU stay in the patient group without bloodstream infection (introducing an important lead time bias), and probably also by differences in baseline characteristics of the patients. To account for differences in exposure time and severity of illness, a matched cohort analysis was performed. In our study, we took particular care that patients had the same diagnosis, severity of illness, age, and gender on ICU admission. Furthermore, control patients were at least as long admitted in the ICU as it took for their respective case patient to develop bloodstream infection. After this adjustment, patients with and without bloodstream infection had an equal length of ICU and hospital stay. Even hospital cost was not different in patients with and without bloodstream infection, although the difference was more pronounced when expressed as hospital costs/hospitalization day; this was still not statistically significant.

The observed mortality was higher than the APACHE II predicted mortality (P < 0.001 for patients with and without bloodstream infection). This is most probably an illustration of the failure of the APACHE II system to predict mortality in a subgroup of ICU patients with ARF.

Using the matched cohort methodology, we also found no significant attributable mortality for bloodstream infection. This was confirmed by the Cox proportional hazard model, in which bloodstream infection was not associated with mortality. Despite the fact that the patients studied had a higher incidence of bloodstream infection, this did not result in a worse survival. These findings conform to our earlier findings and those of others, although not in a renal failure population, that nosocomial bloodstream infection was not associated with increased mortality (18,21–25,27,30,34–36).

An explanation for the absence of attributable mortality can be the high proportion of patients who received adequate antimicrobial therapy and the short delay before its institution. There is ample evidence that these factors can result in differences in survival (37–40). Alternatively, underlying severity of illness could have played a confounding role. It is of note that most of the studies regarding this issue have been undertaken in less severely ill patients, (27,30,31,33–36,41–43) and that no study has yet been accomplished in ARF. It is conceivable that severe disease in general and renal failure as a representative example override the potential effect on survival of bloodstream infection per se.

In the present study, in only 16% of the cases, bloodstream infections could be related to infection of a catheter. Although intravascular catheters, necessary for RRT, pose an increased risk for bloodstream infection, improved catheter management strategies and use of antimicrobial or antiseptic impregnated catheters will probably reduce the incidence of nosocomial bloodstream infections only to a limited extent.


   Conclusions
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
References
 
We found a high incidence of nosocomial bloodstream infections in this large cohort of critically ill patients with ARF who were treated with RRT. With use of the matched cohort analysis technique, we found that nosocomial bloodstream infection had however no effect on the outcome, measured as either length of stay or mortality, in this particular patient group. There was also no difference in total hospital cost between patients with and without bloodstream infection. The high mortality observed in ARF patients could therefore not be attributed to the higher incidence of bloodstream infection.


   Acknowledgments
 
We thank Prof. Verschraegen and Mr. Johan Deschuymer from the Department of Hospital Hygiene for providing the microbiological data, Mrs. Kathleen Kint, pharmacist for providing the pharmacologic data, Mrs. Rose Sypre for secretarial assistance, and Mr. Hubert Loeys for providing the hospital bills. Part of this work was presented at the 43rd ICAAC meeting of the American Society for Microbiology in Chicago, September 14–17, 2003, and the 16th European Society of Intensive Care Medicine annual meeting in Amsterdam, the Netherlands, October 5–8, 2003.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 References
 

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Received for publication September 10, 2003. Accepted for publication November 14, 2003.




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