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1600 CID 2002:34 (15 June) Blot et al.

M A J O R A R T I C L E

Nosocomial Bacteremia Caused by Antibiotic-Resistant Gram-Negative Bacteria in CriticallyIll Patients: Clinical Outcome and Lengthof Hospitalization

Stijn Blot,1 Koenraad Vandewoude,1 Dirk De Bacquer,2 and Francis Colardyn1

1Department of Intensive Care, Ghent University Hospital, and 2Department of Public Health, Ghent University, Ghent, Belgium

Population characteristics and outcomes were retrospectively compared for critically ill patients with noso-

comial bacteremia caused by antibiotic-susceptible (AB-S; ) or antibiotic-resistant (AB-R; )np 208 np 120

gram-negative bacteria. No significant differences in severity of illness and comorbidity factors were seen

between groups. Patients with bacteremia caused by AB-R strains had a longer hospitalization before the onset

of the bacteremia. The in-hospital mortality for patients with bacteremia caused by AB-S strains was 41.8%;

for patients infected with AB-R strains, it was 45.0% ( ). A multivariate survival analysis demonstratedPp .576

that older age ( ), a high-risk source of bacteremia (abdominal and lower respiratory tract;Pp .009 Pp

), and a high acute physiology and chronic health evaluation IIrelated expected mortality ( ) were.031 Pp .032

independently associated with in-hospital mortality ( ). Antibiotic resistance in nosocomial bacteremiaP! .05

caused by gram-negative bacteria does not adversely affect the outcome for critically ill patients.

The widespread use of broad-spectrum antibiotics is

the principal factor in the emergence of antibiotic re-

sistance. Consequently, in intensive care units (ICUs),

where the use of antibiotics is considerably greater than

in general wards [1], dealing with antibiotic-resistant

microorganisms is an almost daily challenge. This must

be considered a major problem, because the develop-

ment of newer and more-potent antibiotics cannotkeep

up with the increase in antibiotic resistance.

In ICUs, gram-negative bacteria are responsible for a

Received 3 December 2001; revised 1 February 2002; electronically published

23 May 2002.

Presented in part: 14th Annual Congress of the European Society of Intensive

Care Medicine, Geneva, 30 September3 October 2001.

Financial support: Fund for Scientific Research, Flanders, Belgium (special

doctoral grant 1.9.205.02N00 to S.B.).

Reprints or correspondence: Dr. Stijn Blot, Dept. of Intensive Care, Ghent

University Hospital, De Pintelaan 185, B-9000 Ghent, Belgium (stijn.blot@rug

.ac.be).

Clinical Infectious Diseases 2002;34:16006

2002 by the Infectious Diseases Society of America. All rights reserved.

1058-4838/2002/3412-0009$03.00

considerable percentage of all bloodstream infections [2].

In ICUs in the United States and Europe, patterns of

reduced susceptibility to antibiotics were found among

gram-negative bacteria [3, 4]. Despite the high prevalence

of antibiotic resistance among gram-negative bacteria

causing bacteremia, the clinical consequences of resis-

tance remain unclear. The main objective of our study

was to evaluate the relationship between antibiotic re-

sistance in gram-negative bacteria causing bacteremia

and the clinical outcomes for critically ill patients. Sec-

ondary objectives were to compare the length of the ICU

stay and hospitalization for patients with bacteremia

caused by antibiotic-susceptible (AB-S) or antibiotic-

resistant (AB-R) gram-negative strains.

METHODS

Setting. This study was performed in the ICU of the

1060-bed Ghent University Hospital in Ghent,Belgium.

The ICU has 54 beds and includes a medical and sur-

gical ICU, an ICU for cardiac surgery, and an ICU for


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Bacteremia Caused by Resistant Microorganisms CID 2002:34 (15 June) 1601

severely burned patients. No significant changes in mean age

of patients, length of the ICU stay, or acute physiology and

chronic health evaluation (APACHE) II score [5] were observed

during the study period.

Study design and data collection. We conducted a retro-

spective, observational cohort study that included ICU patients

with nosocomial, microbiologically documented bacteremia

caused by gram-negative bacteria. We compared data from pa-tients with bacteremia caused by AB-S gram-negative bacteria

with data from patients with bacteremia caused by AB-R gram-

negative bacteria. In-hospital mortality (mortality rate for 3

evaluation points) was the principal outcome variable evalu-

ated. We also assessed secondary outcomes, including length

of stay in the ICU and in the hospital and prevalence of acute

organ failure.

The study included critically ill adult patients who were ad-

mitted to the ICU during a 9-year period (January 1992

December 2000). All microbiologically documented nosoco-

mial bloodstream infections are prospectively screened by the

center for infection control. This hospital-wide case-based sur-

veillance program was used to perform a retrospective search

for ICU patients with bacteremia caused by gram-negative bac-

teria. Every patient whose ICU stay was complicated by this

bloodstream infection was assessed in our analysis. For ICU

patients who developed 11 case of bacteremia caused by gram-

negative bacteria, only the first episode was considered. Patients

with hemocultures that yielded 11 type of gram-negative bac-

teria of which at least 1 strain was AB-R were included in the

AB-R group.

Definitions. Bacteremia was considered to be nosocomial

when it was diagnosed at least 48 h after hospital admission.Gram-negative bacteremia was defined as the presence of

gram-negative bacteria in the blood, documented by at least 1

positive hemoculture. Hemocultures were routinely performed

when the patients temperature was 138.4C or when infection

was suspected on clinical grounds; blood samples were pro-

cessed following the BacT/Alert (Organon Teknika) procedure.

A 10-mL blood culture inoculum was standard. Antibiotic

resistance was defined as in vitro resistance to ceftazidime. In

our hospital, ceftazidime resistance is considered to be an in-

dicator of epidemic extended-spectrum b-lactamaseproducing

strains or hyperproducers ofb-lactamases, and, therefore, it is

a sign of infection with organisms that are resistant to multipledrugs [6, 7]. Because susceptibility patterns for Pseudomonas

aeruginosavary, such isolates were considered to be AB-R when

resistance to one of the following antipseudomonal antibiotics

was seen: piperacillin, ciprofloxacin, ceftazidime, and imipen-

em [8].

Antibiotic resistance was determined according to methods

for disk-diffusion testing recommended by the National Com-

mittee for Clinical Laboratory Standards [9]. For the sake of

convenience, cases of bacteremia were designated AB-S bac-

teremia or AB-R bacteremia, depending on the antibiotic-

resistance status of the isolated organisms. During the study

period, no changes in microbiologic laboratory techniques were

seen. The source of the bacteremia was determined by intensive

care physicians and microbiologists, on the basis of the isolation

of gram-negative bacteria from the presumed portal of entry

and clinical evaluation. For the purpose of analysis, sources ofbacteremia were divided into 3 categories: low risk (associated

mortality, 30%), which were sinus, urinary tract, intravenous

catheter, and soft-tissue sources; intermediate risk (associated

mortality, 31%50%), which were primary sources of bacte-

remia; and high risk (associated mortality, 150%), which were

lower respiratory tract and abdominal sources. Patients with

11 possible source of bacteremia (e.g., 1 low-risk and 1 high-

risk source) were considered to have a high-risk source.

Antibiotic therapy was considered to be appropriate if the

drugs used had in vitro activity against the isolated strain. We

considered antibiotic therapy to be inadequate if the drugs

used did not have in vitro activity against the isolated strainor if the patient did not receive antibiotic treatment. The delay

in the initiation of appropriate antibiotic treatment was cal-

culated from the day of onset of bacteremia. Acute respiratory

failure was defined as ventilator dependence; acute renal fail-

ure, as the need for renal replacement therapy; and hemo-

dynamic instability, as the need for vasopressive or inotropic

support during the ICU stay. For the comparison of outcomes,

survival status was evaluated at 14 and 28 days after the onset

of bacteremia and at the end of the hospital stay (all 3 evaluation

points are included in in-hospital mortality).

Statistical analysis. Continuous variables are given as

or as median (lowerupper quartile), dependingmean SD

on the distribution. Comparative analyses were done with the

Mann-WhitneyUtest or the x2 test, as appropriate. Survival

curves were prepared by means of the Kaplan-Meier method,

and univariate survival distributions were compared by the log-

rank test. To assess the relationship between in-hospital mor-

tality and a set of independent variables, a multivariate survival

analysis was used (Cox proportional hazard model); hazard

ratios and 95% CIs are reported. In this multivariate analysis,

continuous variables were handled continuously. Variables en-

tered in the Cox regression model were required to have a

plausible relationship with mortality, to avoid spurious asso-

ciations. Statistical analyses were performed using Statistica,

version 4.5 (StatSoft), and SPSS, version 9.0. All tests were 2

tailed; was considered to be statistically significant.P! .05

RESULTS

During the study period, 29,727 patients were admitted to the

ICU. Among these, 328 patients were identified as havinggram-


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Table 1. Characteristics of hospitalized, critically ill patients who had nosocomial bacteremia caused by gram-negative bacteria.

Characteristic

Outcome of hospital stay Type of bacteremia

Death

(n p 141)

Survival

(n p 187) P

AB-S

(n p 208)

AB-R

(n p 120) P

Age, mean years SD 59 14.3 49 18.1 !.001 54 17.4 52 16.9 .303

APACHE II score, mean SD 26 9.4 22 8.0 !.001 23 9.0 23 8.6 .814

APACHE IIrelated expected mortality, mean %

SD 50 29.0 36 25.1 !.001 41 28.2 44 27.3 .305

Acute renal failure, % of patients 38.3 16.0 !.001 25.0 26.7 .431

Hemodynamic instability, % of patients 86.5 75.9 .017 77.9 85.0 .117

Acute respiratory failure, % of patients 95.7 92.0 .021 92.4 95.8 .227

Ventilator dependence, median days (lowerupper

quartile) 17 (628) 21 (834) .165 16 (527) 23 (1238) !.001

Length of ICU stay, median days

(lowerupper quartile)

Before onset of bacteremia 10 (318) 13 (624) .009 8 (3.517) 18 (933) !.001

After onset of bacteremia 8 (317) 12 (525) .002 10 (319) 11 (520) .321

Total 18 (934) 28 (1446) !.001 21 (940) 28.5 (1648) !.001

Length of hospitalization, median days

(lowerupper quartile)Before onset of bacteremia 13 (527) 16 (727) .428 11 (522) 23 (1141) !.001

After onset of bacteremia 10 (321) 59 (28117) !.001 27 (963.5) 35 (1077) .333

Total 29 (1554) 76 (44144) !.001 47 (2285) 60 (30130) .007

Mortality at 14 days, % of patients 61.0 0 26.0 26.7 .550

Mortality at 28 days, % of patients 81.0 0 34.1 35.8 .756

In-hospital mortality, % of patients 100 0 41.8 45.0 .576

NOTE. AB-R, antibiotic resistant; AB-S, antibiotic susceptible; APACHE, acute physiology and chronic health evaluation; ICU, intensive care unit.

negative bacteremia and were included in the study cohort (a

prevalence of 11.0 cases of gram-negative bacteremia per 1000

ICU admissions). The mean age of the patients was 54years. The mean APACHE II score was , and the17.2 23 8.9

mean APACHE IIrelated expected mortality was 42%

. Fifty-four percent of the patients were admitted to the27.8%

ICU after a surgical procedure; 75% of these patients had non-

elective surgery. Twenty percent of the patients were admitted

after experiencing trauma.

Among the 328 cases of bacteremia included in the analysis,

369 gram-negative isolates were identified. The most frequently

detected gram-negative microorganisms were Escherichia coli

( ), Enterobacter species ( ), P. aeruginosa (np 71 np 68 np

),Klebsiellaspecies ( ),Acinetobacterspecies ( ),62 np 52 np 51

and Serratia species ( ). In 36.6% (120 of 328) of thenp 27

cases of bacteremia, the strain involved was AB-R. During the

study period, the yearly rate of AB-R bacteremia remained

stable ( ) (data not shown).Pp .495

Outcome of hospital stay. Mortality rates at 14 days, at

28 days, and at the end of the hospital stay were, respectively,

26%, 35%, and 43%. The characteristics of the patients who

died in the hospital and the characteristics of those who sur-

vived are compared in table 1. Patients who died in the hospital

generally were older and had higher APACHE II scores and

APACHE IIrelated expected mortality, and the prevalence oforgan failure was also higher in this group. These patients had

a shorter ICU stay and a shorter hospitalization. Of all bac-

teremia-associated factors, only infection with P. aeruginosa

and high-risk sources of bacteremia were more prevalentamong

nonsurvivors (table 2).

Patients with AB-S bacteremia versus those with AB-R bac-

teremia. The population characteristics of patients with AB-

S gram-negative bacteremia and those with AB-R gram-neg-

ative bacteremia are listed in tables 1 and 2. Polymicrobial

bloodstream infections were more likely to occur in the AB-

R group. Furthermore, no important differences in severity

of illness were found, but patients with AB-R bacteremia had

a longer stay in the ICU, as well as in the hospital. This seems

to be the consequence of a longer hospitalization before the

onset of the bacteremia; length of stay (both in ICU and

hospital) after the onset of the bacteremia was not different.

Antibiotic resistance was not associated with higher mor-

tality rates (table 1). Figure 1 shows the survival curves for

both groups from the onset of bacteremia to the end of hos-


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Table 2. Factors associated with bacteremia in a study of hospitalized, critically ill patients with nosocomial

bacteremia caused by gram-negative bacteria.

Factor

Outcome of hospital stay Type of bacteremia

Death

(n p 141)

Survival

(n p 187) P

AB-S

(n p 208)

AB-R

(n p 120) P

AB-R bacteremia 38.3 35.3 .576

Isolated microorganism

Escherichia coli 21.3 21.9 .888 30.8 5.8 !.001

Enterobacterspecies 17.0 23.5 .150 14.4 31.7 !.001

Pseudomonas aeruginosa 27.0 12.8 .001 18.8 19.2 .926

Klebsiellaspecies 12.7 18.2 .184 15.9 15.8 .994

Acinetobacterspecies 12.1 17.6 .163 4.8 33.3 !.001

Serratiaspecies 9.2 7.5 .572 9.6 5.8 .230

Polymicrobial bloodstream infection 33.3 26.2 .160 24.5 37.5 .013

Source of the bacteremia

Low risk 17.0 41.2 !.001 33.7 27.5 .247

Intermediate risk 22.7 25.1 .609 20.7 30.0 .060

High risk 60.3 32.6 !.001 45.7 42.5 .578

More than 1 possible source 9.2 10.0 .901 7.7 12.5 .152

Appropriate antibiotic therapy 89.3 94.6 .108 93.1 91.1 .547

Delay in antibiotic therapy, mean days SD 0.5 0.9 0.7 1.6 .296 0.5 0.8 0.8 2.0 .556

NOTE. Data are percentage of patients, unless otherwise indicated. AB-R, antibiotic resistant; AB-S, antibiotic susceptible.

Figure 1. Survival curves for patients in the intensive care unit who had bacteremia caused by antibiotic-susceptible(dashed line)or antibiotic-

resistant (solid line)gram-negative bacteria ( ; log-rank test).Pp .319

pitalization. The mortality rates for the 2 groups were very

similar ( ). At the end of the hospitalization period,Pp .319

mortality rates for patients with AB-S bacteremia and those

with AB-R bacteremia were, respectively, 41.8% and 45.0%

( ). To adjust for differences in clinical virulence, out-Pp .576

come comparisons for the 2 groups of patients were per-

formed, according to the different types of gram-negative mi-

croorganisms involved. When patients were stratified by

most-prevalent bacteria, no statistically significant difference

in mortality was seen between the 2 groups ( ; table 3).P1.05

Multivariate survival analysis. A multivariate survival

analysis demonstrated that older age, a high-risk source of

bacteremia, and a high APACHE IIrelated expected mortality

were independently associated with in-hospital mortality (ta-


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Table 3. Mortality rates among hospitalized, critically ill pa-

tients with bacteremia caused by gram-negative bacteria, strat-

ified by most frequently detected microorganism and distributed

by antibiotic-resistance status of the isolate.

Microorganism,

resistance status

No. of

isolates

Mortality, no. (%) of patients

At 14 days At 28 days Total

Escherichia coli

AB-S 64 14 (21.9) 20 (31.3) 25 (39.1)

AB-R 7 4 (57.1) 4 (57.1) 5 (71.4)

Enterobacterspecies

AB-S 31 7 (22.6) 9 (29.0) 11 (35.5)

AB-R 37 7 (18.9) 9 (24.3) 13 (35.1)

Pseudomonas

aeruginosa

AB-S 39 12 (30.8) 17 (43.6) 25 (64.1)

AB-R 23 9 (39.1) 11 (47.8) 13 (56.5)

Klebsiellaspecies

AB-S 34 6 (17.6) 9 (26.5) 9 (26.5)

AB-R 18 5 (27.8) 8 (44.4) 9 (50.0)

Acinetobacterspecies

AB-S 10 0 1 (10.0) 1 (10.0)

AB-R 41 8 (19.5) 14 (34.1) 17 (41.5)

Serratiaspecies

AB-S 21 7 (33.3) 10 (47.6) 10 (47.6)

AB-R 6 3 (50.0) 3 (50.0) 3 (50.0)

NOTE. Differences in mortality for patients withantibiotic-susceptible(AB-

S) and patients with antibiotic-resistant (AB-R) bacteremia did not reach sta-

tistical significance at any time point ( ).P! .05

Table 4. Factors associated with in-hospital mortality among

hospitalized, critically ill patients with bacteremia caused by

gram-negative bacteria.

Variable Hazard ratio (95% CI) P

Age 1.01 (1.001.02) .009

High-r isk source of bacteremia 1.33 (1.031.72) .031

APACHE IIrelated expected

mortality 1.71 (1.052.79) .032

Acute renal failure 1.32 (0.981.76) .065

Pseudomonas aeruginosa

bacteremia 1.33 (0.961.85) .085

NOTE. Associations were assessed using multivariate survival analysis

(Cox proportional-hazard model). APACHE, acutephysiology and chronic health

evaluation.

ble 4). Acute renal failure and bacteremia caused byP. aeru-

ginosahad an association with in-hospital mortality that wasof borderline significance ( ).P!.1

DISCUSSION

It is presumed that infections caused by AB-R bacteria result

in higher mortality, longer hospitalizations, and greater costs

than do infections caused by AB-S bacteria, although few data

support this intuitive concept [10]. The assumption that in-

fections caused by AB-R bacteria are associated with a higher

mortality rate may be based on the possibility that appropriate

antibiotic therapy will be initiated later for such infections than

for infections caused by AB-S bacteria. Although some studies

have described very high mortality rates in association with

infections caused by AB-RP. aeruginosaand Acinetobacter bau-

mannii[8, 11], the causal link between antibiotic resistance and

fatal bacteremia remains unclear.

Comparisons of the outcomes for patients with AB-R bac-

teremia and for patients with AB-S bacteremia can be difficult

to perform: important differences in demographic character-

istics between the populations are repeatedly observed in stud-

ies of bacteremia caused by AB-R gram-positive bacteria

[1214]. In the present study, no important differences in

severity of illness (as measured by the APACHE II score) or

prevalence of acute organ failure hampered the outcome com-

parison. Polymicrobial bloodstream infections were seen more

frequently among patients with AB-R bacteremia. Although

this is considered to be an ominous sign [15, 16], it has been

demonstrated elsewhere that the mortality associated withpolymicrobial bacteremia in ICU patients is not necessarily

higher than that associated with monomicrobial bacteremia

[17]. In our study, polymicrobial bacteremia was not asso-

ciated with higher in-hospital mortality on either univariate

or multivariate analysis.

Our data revealed that the mortality associated with AB-R

gram-negative bacteremia is not higher than that associated

with AB-S bacteremia. Although mortality is high in both

groups of patients, the observed mortality rates are in line with

the APACHE IIrelated expected mortality. In a retrospective

study, Menashe et al. [18] also found no significant increase in

mortality among patients with bacteremia caused by extended-spectrumb-lactamaseproducing Enterobacteriaceae (50%, vs.

38% among patients with bacteremia caused by nonextended-

spectrumb-lactamaseproducing isolates; ), but theirPp .367

study cohort was small ( ). Harbarth et al. [16], in anp 55

large retrospective study, also failed to demonstrate that anti-

biotic resistance had a major clinical effect on outcome for

patients with gram-negative bacteremia. However, the hospital-

wide setting and large proportion of cases of community-

acquired bacteremia (61%) in that study hampers comparison

with the results we obtained.

Previous studies have identified important associations be-

tween antibiotic resistance and negative outcome for patients

with gram-negative bacteremia [1921]. However, causality re-

mains unclear, and differences in study populations impede

comparison with the present study.

It is a possible weakness in our study that the outcome

comparison between the 2 groups of patients might be con-


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founded by differences in the clinical virulence of the types of

gram-negative bacteria involved [16]. For example, 80% ofAci-

netobacter species, which are considered to be low-virulence

pathogens, were AB-R, whereas 37% ofPseudomonasisolates,

which are known to be extremely virulent, were AB-R. Re-

gardless, in the multivariate survival analysis, no individual

microorganism was recognized as being an independent pre-

dictor of mortality. Therefore, we assume that the confoundingeffect of differences in clinical virulence of the different types

of bacteria seen in our study is of minor importance. However,

outcome evaluation after stratification for different bacteria can

be interesting.

In a prospective cohort study involving patients with bac-

teremia caused exclusively byEnterobacterspecies, Chow et al.

[21] describe greater morbidity and mortality among patients

with bacteremia caused by AB-REnterobacterspecies. Our study

included 68 ICU patients with bacteremia caused byEntero-

bacter, 37 of whom were infected with AB-R strains. Although

these numbers are small and, therefore, are difficult to interpret,

the mortality rates in these subgroups were nearly equal (35.5%

and 35.1%, respectively), raising doubts about whether a worse

prognosis was associated with bacteremia caused by AB-REn-

terobacterspecies in our population. Also, when data were strat-

ified by other frequently detected gram-negative microorgan-

isms, no statistically significant differences in the mortality rates

were found for the AB-S group and the AB-R group (table 3).

Nonetheless, the differences in the mortality rates for patients

with bacteremia caused by AB-S or AB-R strains ofKlebsiella

species, E. coli, and, in particular, Acinetobacterspecies, which

reached borderline significance ( ), are noteworthy. TheseP! .1

results, however, must be interpreted cautiously because of thesmall numbers of patients included.

It can be presumed that bacteremia caused by AB-R bacteria

may have a worse prognosis because of the delay in initiation

of appropriate antibiotic therapy [22, 23]. Especially when high-

virulence microorganisms such as P. aeruginosa are involved,

early initiation of appropriate therapy is crucial to the survival

of the patient [24, 25]. In our study, patients with AB-R bac-

teremia were treated appropriately at a rate similar to that for

patients with AB-S bacteremia. The delay in the initiation of

appropriate treatment was longer in the AB-R group, but the

difference we found was of no significance, either statistically

or clinically (table 2).The high rate of administration of appropriate therapy that

was achieved in our ICU population can be explained by 3

factors: (1) consideration of previous colonization, as assessed

by regular site-specific surveillance cultures (3 times weekly),

(2) initial administration of broad-spectrum antibiotic therapy,

and (3) close interaction between the physician, clinical mi-

crobiologists, and clinical infectious diseases consultants. This

strategy appeared to contribute to a delay in administration of

appropriate antibiotic treatment that was short (!1 day) overall

in our study. Surveillance sampling was found to have a high

specific and negative predictive value, because colonization pre-

ceded infection in almost all patients who had P. aeruginosa

infection in the ICU [26, 27]. On the other hand, performing

surveillance cultures routinely is expensive. Furthermore,

whether this policy has greater clinical benefits than does ini-

tiation of blind therapy with broad-spectrum antibiotics is stillcontroversial. It is well understood that blind therapy is re-

stricted to a smaller spectrum, once microbiologic identification

is completed, yet it might be assumed that this promotes the

emergence of AB-R microorganisms, because there is more

exposure to broad-spectrum antibiotics. Our strategy is to re-

serve these agents for patients with sepsis whose condition is

deteriorating and for whom no isolate has been obtained from

the presumed septic focus and for patients who have micro-

biologically proved superinfection.

Patients with AB-R bacteremia had a significantly longer stay

in the ICU, as well as in the hospital. However, when length

of ICU stay and length of hospitalization (from the day of theonset of bacteremia to discharge or death) were compared, no

difference was found. We conclude from this that the excess

length of stay, both in the ICU and the hospital, is a result of

a longer ICU and hospital stay before the onset of the bacte-

remia. Consequently, it appears that cases of AB-R bacteremia

are not responsible for the increased need for hospital resources

among these patients but that risk factors for the acquisition

of AB-R infections are the major triggers of this problem.

In conclusion, we found that AB-R gram-negative bacteremia

is not associated with higher mortality than is AB-S gram-

negative bacteremia in critically ill patients. AB-R bacteremia

is associated with a longer stay in the ICU, as well as in the

hospital. This, however, is the consequence of a longer stay

before the onset of the bacteremia, whereas length of stay in

the ICU and length of stay in the hospital after onset of the

bacteremia in the 2 group of patients were not different.

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