Word count (abstract): 245
Word count (text): 2463
Does catheter-associated urinary tract infection increase mortality in critically ill patients?
Christophe Clec’h, MD,
Medical-surgical intensive care unit, Avicenne teaching hospital, Bobigny, France.
Outcome of cancer and criticall illnesses, INSERM/UJF U823, Albert Bonniot institute, Rond point de la
Chantourne, 38706 La Tronche Cedex, France.
Carole Schwebel, MD, medical intensive care unit, Albert Michallon teaching hospital, Grenoble, France.
Adrien Français, biostatistician, department of epidemiology, INSERM U823, Grenoble, France.
Dany Toledano, MD, medical intensive care unit, hospital of Gonesse, Gonesse, France.
Jean-Philippe Fosse, MD, medical-surgical intensive care unit, Avicenne teaching hospital, Bobigny, France.
Maïté Garrouste-Orgeas, MD, medical intensive care unit, Saint-Joseph hospital, Paris, France.
Elie Azoulay, MD, PhD, medical intensive care unit, Saint-Louis teaching hospital, Paris, France.
Christophe Adrie, MD, PhD, medical intensive care unit, Delafontaine hospital, Saint-Denis, France.
Samir Jamali, MD, medical-surgical intensive care unit, hospital of Dourdan, Dourdan, France.
Adrien Descorps-Declere, MD, surgical intensive care unit, Antoine Béclère teaching hospital, Clamart, France.
Didier Nakache, computer scientist, Conservatoire National des Arts et Métiers (CNAM), Paris, France.
Jean-François Timsit, MD, PhD, Outcome of cancer and criticall illnesses, INSERM/UJF U823, Albert Bonniot
institute, Rond point de la Chantourne, 38706 La Tronche Cedex, France.
Yves Cohen, MD, medical-surgical intensive care unit, Avicenne teaching hospital, Bobigny, France.
On behalf of the OUTCOMEREA study group. Members of the OUTCOMEREA study group are listed in the
appendix.
Potential conflicts of interest. All authors: no conflict to disclose.
Financial support. The French Ministry of Science and Technique (grant RNTS 03-2-93-0513).
Running head: impact of urinary tract infection.
1
Correspondence and requests for reprints should be addressed to:
Dr Christophe Clech, INSERM U823, team: Outcome of cancer and critical illnesses, Albert Bonniot Institue, Rond
point de la Chantourne 38706 La Tronche Cedex.
Phone: +33148955249/ Fax: +33148955090. E-mail: christophe.clech@avc.aphp.fr
ABSTRACT
OBJECTIVE. To yield an accurate estimation of the association of catheter-associated urinary tract infection
(CAUTI) with intensive care unit and hospital mortality, controlling for major confounding factors.
DESIGN. Nested case-control study in a multi-center cohort (the OUTCOMEREA database).
SETTING. Twelve French medical or surgical intensive care units.
PATIENTS. All patients admitted between January 1997 and August 2005 requiring the insertion of an indwelling
urinary catheter. Patients who developed CAUTI (cases) were matched to controls according to the following
criteria: sex, age ± 10 years, SAPS (Simplified Acute Physiology Score) II score ± 10 points, length of urinary tract
catheterization, and presence or absence of diabetes mellitus. The association of CAUTI with ICU and hospital
mortality was assessed using conditional logistic regression.
RESULTS. Of the 3281 patients with an indwelling urinary catheter, 298 (9 %) developed at least one episode of
CAUTI. The incidence density of CAUTI was 12.9 per 1000 catheterization days. Crude ICU and hospital mortality
rates were higher in patients with than in those without CAUTI (32% vs 25%, p = 0.02, and 43% vs 30%, p < 0.01,
respectively). After matching and adjustment, CAUTI was no longer associated with increased mortality (ICU
mortality: odds ratio -OR-: 0.846, 95% confidence interval -CI-: 0.659-1.086, p = 0.19; hospital mortality: OR:
0.949, 95% CI: 0.763-1.181, p = 0.64).
CONCLUSION. After careful controlling for confounding factors, CAUTI was not associated with an excess in
either ICU or hospital mortality in our population of critically ill patients.
2
3
1
INTRODUCTION
2
3
4
Urinary tract infections (UTI) are the most common infection acquired in hospitalized adult patients, accounting for
5
30-40 % of all nosocomial infections.1, 2 Within the hospital, the intensive care unit (ICU) has the highest prevalence
6
of UTI (8-21%), more than 95 % of which being associated with the presence of an indwelling urinary catheter. 3, 4
7
Although catheter-associated urinary tract infection (CAUTI) being a very common issue, its link with mortality
8
remains controversial. In a large cohort study conducted in 1982, Platt et al. reported a significantly higher risk of
9
hospital mortality in patients with CAUTI.5 Two more recent studies found similar results.6, 7 Three other studies,
10
however, reported opposite results stating that CAUTI did not increase mortality. 8-10 Discrepant results of these
11
studies could be ascribable to patients’ baseline heterogeneousness and subsequent in-hospital events, which may
12
have confounded the link between CAUTI and mortality.
13
Knowing the real impact of CAUTI on patients’ outcome is undoubtedly necessary to decide whether specific
14
treatments are required. Particularly, it would help resolve some important issues frequently arising in the ICU such
15
as the need to change the urinary catheter or give antibiotics.
16
Thus, we performed this study to yield a more accurate estimation of the association of CAUTI with ICU and
17
hospital mortality, matching patients on the probability of ICU-acquired UTI, and further controlling for major
18
confounding factors.
19
20
21
METHODS
22
23
24
Study Design and Data Source
25
We conducted a nested case-control study in a multi-center cohort (the OUTCOMEREA database) from January
26
1997 to August 2005. The database, fed by 12 French ICUs, is designed to record daily disease severity and
27
occurrence of iatrogenic events. A random sample of patients older than 16 years and having ICU stays longer than
3
28
24 h was entered into the database each year. Briefly, each participating ICU could choose between two sampling
29
methods: (1) consecutive admissions in n randomized beds or (2) consecutive admissions in a randomized month.
30
In accordance with French law, the OUTCOMEREA database was declared to and approved by the Commission
31
Nationale de l’Informatique et des Libertés (CNIL). Since routine collection of clinical and paraclinical data did not
32
modify patients’ management in anyway and statistical analyses were processed anonymously, informed consent for
33
participation in the study was waived.
34
35
Method of data collection
36
Senior physicians of the participating ICUs closely involved in establishing the database collected data daily. For
37
each patient, the investigators entered the data into a computer case-report form using the data capture software
38
VIGIREA (OUTCOMEREATM, Rosny-sous-Bois, France) and imported all records to the OUTCOMEREA
39
database. All codes and definitions were written before data collection.
40
41
Quality of the database
42
The data capture software immediately conducted an automatic check of most of the variables entered by the
43
investigators. Multiple automatic checking of internal consistency generated queries that were sent to the ICUs
44
before the new data were incorporated into the database. At each participating ICU, the quality control procedure
45
involved having a senior physician from another participating ICU check a 2% random sample of study data. Kappa
46
coefficients ranged from 0.5 to 0.9 for qualitative variables, and inter-rater correlation coefficients ranged from 0.67
47
to 1 for clinical variables, severity scores, and organ dysfunction scores.
48
The lowest kappa coefficient was obtained for Mc Cabe score. The lowest inter-rater correlation was obtained for
49
lactate level on day 3. Otherwise, the kappa coefficient was always higher than 0.62 for qualitative variables, and the
50
inter-rater coefficient ranged between 0.72 and 0.99 for quantitative variables. In particular, it ranged between 0.78
51
and 0.91 for severity and organ dysfunction scores, and was 0.99 for duration of mechanical ventilation, ICU and
52
hospital stay.”
53
54
Study Population and definitions
4
55
All patients in the database were eligible. Patients with UTI before insertion of the urinary catheter, and patients
56
without urinary catheter were excluded.
57
Patients were cautiously screened for CAUTI. Specimens were systematically collected for urine cultures, either on
58
a weekly basis, or if a new sepsis occurred. CAUTI was deemed present when urine cultures yielded at least 103
59
cfu/ml of one or two microorganisms.11, 12 A bacteremic/fungemic CAUTI was defined as a CAUTI with positive
60
blood cultures with the same microorganism within a 48 hours period.
61
Patients who developed CAUTI represented the cases. In patients who developed several episodes of CAUTI, only
62
the first episode was included in the analysis. Controls were selected among the remaining patients. Cases were
63
matched to controls on the basis of predicted mortality and known risk factors for ICU-acquired UTI,13-17 using the
64
algorithm available on line at: http://www.outcomerea.org/ehtm/matchmacro.pdf. More precisely, matching criteria
65
were as follows: sex, age ± 10 years, SAPS (Simplified Acute Physiology Score) II ± 10 points, presence or absence
66
of diabetes mellitus, and length of urinary tract catheterization. In addition, we imposed that the time to CAUTI
67
from the insertion of the urinary catheter in the cases be less or equal than the length of urinary tract catheterization
68
of their respective controls.
69
70
Data Collection
71
The following data were collected: age, sex, Mc Cabe class (class 1, no fatal underlying disease; class 2, underlying
72
disease fatal within 5 years; class 3, underlying disease fatal within 1 year),18 comorbidities assessed according to
73
the Acute Physiology and Chronic Health Evaluation (APACHE) II definitions, 19 severity of illness at ICU
74
admission and daily during the ICU stay assessed using the SAPS II score,20 the Sequential Organ Failure
75
Assessment (SOFA) score 21 and the Logistic Organ Dysfunction (LOD) score, 22 admission category (medical,
76
scheduled surgery, or unscheduled surgery), admission diagnosis, whether the patient was transferred from a ward
77
(defined as a stay in an acute-bed ward ≥24 hours immediately before ICU admission), lengths of ICU and hospital
78
stays, and vital status at ICU and hospital discharge. Invasive procedures (placement of an arterial or central venous
79
catheter, and endotracheal intubation), treatments of organ failure (catecholamine infusion, mechanical ventilation),
80
and antibiotic use were also recorded.
81
82
Statistical Analyses
5
83
Comparisons between patients in the whole cohort were based on chi-square tests for categorical data and on
84
Wilcoxon’s test for continuous data.
85
Assuming an ICU mortality of 30% in patients without CAUTI, and that CAUTI would occur in more than 250
86
patients, we calculated that 3 controls per patient with CAUTI would be necessary to unmask a difference in the
87
odds ratio of mortality of 1.5 with an alpha risk of 5% and a power of 80%.
88
Comparisons between matched patients were first based on bivariate conditional logistic regression. Multivariate
89
conditional logistic regression was then used to examine the association between CAUTI and ICU and hospital
90
mortality, adjusting for potential confounding variables (ie, variables that had a p value ≤.10 in bivariate analysis).
91
Wald 2 tests were used to determine the significance of each variable. Adjusted odds ratios (OR) and 95%
92
confidence intervals (CI) were calculated for each parameter estimate.
93
A p value less than .05 was considered significant. Analyses were computed using the SAS 9.1 software package
94
(SAS Institute, Cary, NC, USA).
95
96
97
RESULTS
98
99
100
Study population
101
Of the 4811 OUTCOMEREA database patients, 64 (1.3 %) had urinary tract infection on ICU admission and were
102
excluded. Among the remaining 4747 patients, 3281 (69.1 %) had an indwelling urinary catheter and 298 (9%) had
103
CAUTI. The overall incidence density of CAUTI was 12.9 per 1000 catheterization days. Bacteremic/fungemic
104
CAUTI occurred in 4 cases for an overall incidence density of 0.17 per 1000 catheterization days. The median
105
[interquartile range] time to CAUTI was 11 [6-19] days from the insertion of the urinary catheter.
106
On the day CAUTI occurred, 64 (21.5 %) patients required catecholamine infusion and 198 (66.4 %) patients were
107
receiving antibiotics for extra-urinary sepsis. General characteristics of study patients are shown in table 1.
108
Several factors present at admission or within 48 hours of ICU stay were associated with an increased risk of
109
CAUTI. Patients with CAUTI, as compared to those without CAUTI, were older, had higher SAPS II scores and
6
110
were more likely to have received catecholamine infusion or mechanical ventilation during the first 48 hours of ICU
111
stay (table 1).
112
113
Microbiology
114
Two hundred thirty-two (77.8%) patients had one episode of CAUTI, 44 (14.8%) patients had two episodes, and 22
115
(7.4%) patients had three or more episodes. Most episodes (93.6%) were monomicrobial. Microorganisms retrieved
116
from urine cultures are listed in table 2. Microorganisms identified both in urine and blood cultures were:
117
Pseudomonas aeruginosa, Proteus mirabilis, Escherichia coli, and Candida albicans.
118
119
Matching
120
Among the 298 patients with CAUTI, 273 (91.6%) were matched successfully to 896 controls for all matching
121
criteria. Unmatched patients were younger and had longer length of urinary catheterization than matched patients
122
but had similar SAPS II and LOD scores at ICU admission.
123
Cases were less likely than controls to have received antibiotics within 72 hours before CAUTI (or the
124
corresponding day in controls). General characteristics and in-ICU events potentially associated with mortality in
125
cases and controls are shown in table 3.
126
127
Outcomes
128
Overall, ICU and hospital mortality rates in patients with and without CAUTI were 32% vs 25% (p = .02) and 43%
129
vs 30% (p < .01), respectively. Lengths of ICU and hospital stays (median in days, interquartile range) were
130
significantly increased in patients with than in those without CAUTI (28 16-45 vs 7 4-13, p<0.001, and 51 30-
131
80 vs 20 10-38, p<0.001, respectively).
132
After matching on risk factors for CAUTI, unadjusted analysis revealed that CAUTI did not worsen ICU or hospital
133
survival (table 4). Lengths of ICU and hospital stays (median in days, interquartile range) remained significantly
134
increased in patients with than in those without CAUTI (26 16-43 vs 13 8-23, p<0.0001, and 49 29-78 vs 29
135
18-54, p<0.0001, respectively). After further adjustment on confounding factors (namely: septic shock, multiple
136
organ failure and coma as reason for ICU admission, mechanical ventilation during the first 48 hours of ICU stay,
137
extra-urinary sepsis, and antibiotic use) there was still no difference in ICU and hospital survival (table 4).
7
138
139
140
DISCUSSION
141
142
143
Development of a nosocomial UTI is a common complication among ICU patients requiring urinary catheterization.
144
Several studies have evaluated the risk of death associated with nosocomial UTI, but only a few of them specifically
145
focused on ICU patients.6, 7, 9 This study is one of the largest to have evaluated the impact of CAUTI on ICU and
146
hospital mortality. Crude mortality was higher in patients with than in those without CAUTI but there was no more
147
excess in mortality after careful matching and adjustment on confounding factors.
148
In a widely cited prospective cohort study, Platt et al. found a significantly increased risk of hospital mortality in
149
patients with CAUTI.5 Nevertheless, they did not focus on ICU patients and it was not clear whether mortality was
150
indeed attributable to CAUTI. More recently, Rosenthal et al. also reported an increased risk of mortality due to
151
ICU-acquired UTI, but they did not adjust for potentially important confounding factors including severity of
152
illness.6 Another study showed similar results.7 After controlling for confounding factors, Laupland et al. concluded
153
that ICU-acquired UTI was not a significant attributable cause of mortality. 9 However, confounding factors adjusted
154
for were not well defined and patients in this study may have been heterogeneous with regard to the probability of
155
ICU-acquired UTI.
156
In our study, we dealt with heterogeneousness more extensively by matching patients on predicted mortality and
157
known risk factors for CAUTI.13-17 Moreover, we clearly defined and adjusted for confounding factors. Thus, we
158
were able to identify more precisely the independent effect of CAUTI on mortality. The conclusion that CAUTI did
159
not worsen patients’ outcome has potentially important implications for the management of patients with an
160
indwelling urinary catheter. First, systematic urine cultures in patients with an indwelling urinary catheter may be
161
unnecessary and, consequently, unduly costly. Second, systematic changing of urinary catheter in case of CAUTI
162
may not be recommended, all the more as it could be associated with septicemia. Finally, CAUTI could be
163
considered as colonization rather than infection, and antibiotics should not be given in the absence of associated
164
bacteremia/fungemia (which is a rather rare occurrence anyway), pyelonephritis, or prostatitis. Antibiotics seem to
165
decrease the risk of CAUTI, but, conversely, the absence of antibiotics does not seem to have a negative impact.
8
166
Some limitations of this study merit consideration. First, the observational design of our study precludes making any
167
definite recommendation. Further prospective interventional studies are needed to confirm our findings. Specifically,
168
these studies should assess the impact of urinary catheter changing and antibiotic therapy in patients with CAUTI.
169
Second, there might be some “masked” confounding factors since this was not a controlled study. But, by matching
170
on known risk factors for ICU-acquired UTI and controlling for usual risk factors for mortality, we dealt with
171
confounding more extensively than any prior report.
172
Third, not all patients with CAUTI could be matched. Yet, the proportion of non-matched patients was very low in
173
spite of the large number of matching criteria, and those patients had the same probability of death as defined by
174
usual severity scores on ICU admission. So, it is very unlikely to have changed the results.
175
Fourth, we did not define CAUTI according to the Centers for Disease Control and Prevention (CDC) criteria for
176
nosocomial infections.23 However, the CDC definition is difficult to apply to the ICU setting: functional signs are
177
impossible to identify in sedated patients with an indwelling urinary catheter, fever is either lacking or unspecific,
178
and bacterial growth may be impaired by ongoing antibiotic therapy for extra-urinary sepsis. Thus, most episodes of
179
CAUTI are asymptomatic. That is why we had to systematically collect specimens for urine cultures on a weekly
180
basis or when a new sepsis occurred. That the overall incidence density of CAUTI and bacteremic/fungemic CAUTI
181
was consistent with previous reports shows the diagnosis of CAUTI was neither overestimated nor underestimated
182
in our study.9, 24-26
183
Fifth, one may argue that the implementation of a specific treatment (urinary catheter changing and antibiotic
184
therapy) might reduce ICU and hospital lengths of stay in patients with CAUTI. It must be emphasized, however,
185
that the benefits of such a treatment are hypothetical. Additionally, longer lengths of stay observed in this study
186
were probably related to more severe underlying conditions and disease severity rather than to CAUTI itself.
187
Sixth, that most patients with CAUTI were on antibiotic therapy may also have confounded the results by protecting
188
patients against septic shock and death. Nevertheless, those factors were adjusted for, and patients with CAUTI
189
received fewer antibiotics than their respective controls.
190
Finally, it must be kept in mind that the prognosis of CAUTI may depend on the microorganisms involved.
191
Particularly, the risk of death may be increased in case of candiduria. 27 Other pathogens such as Pseudomonas
192
aeruginosa or Escherichia coli may also carry a higher risk of death. This issue remains to be clarified.
9
193
In conclusion, CAUTI does not seem to increase mortality in ICU patients after careful matching and controlling for
194
confounding factors. Further prospective interventional studies are required to confirm our results.
10
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13
TABLE 1. General characteristics of patients with and without CAUTI
Variable
Pa
Patients with CAUTI
Patients without CAUTI
(n = 298)
(n = 2983)
69 57-77
66 51-76
.001
160 (54)
1831 (61)
.10
46 36-57
42 30-57
.014
5 3-7
4 2-7
.12
Medical
186 (62)
1862 (62)
Scheduled surgery
38 (12)
484 (16)
Unscheduled surgery
74 (25)
637 (21)
Cardiac disease
51 (17)
467 (16)
.51
Respiratory Disease
62 (21)
496 (17)
.07
Renal Disease
6 (2)
100 (3)
.22
Liver Disease
17 (6)
170 (6)
.99
Immunodeficiency
39 (13)
371 (12)
.75
Uncomplicated diabetes mellitus
50 (17)
463 (16)
.57
Complicated diabetes mellitus
17 (6)
126 (4)
.23
Catecholamine infusion
164 (55)
1369 (46)
.01
Mechanical ventilation
137 (46)
923 (31)
< .01
Use of antibiotics
224 (74)
2203 (73)
.91
Use of broad-spectrum antibiotics
163 (54)
1665 (56)
.71
Age, years, median IQR
Males
SAPS II score, median IQR
LOD score, median IQR
Admission category
.12
Chronic coexisting conditions
First 48 hours in the ICU
NOTE. Data are expressed as number (%), unless otherwise indicated. IQR, interquartile range; SAPS II, Simplified
Acute Physiology Score version II; LOD, Logistic Organ Dysfunction.
a
Wilcoxon’s test for continuous data, and chi-square test for categorical data.
14
TABLE 2. Microbial etiologies of CAUTI
Microorganism
Number (% of episodes)
Escherichia coli
88 (29.5)
Candida species
85 (28.5)
Pseudomonas aeruginosa
54 (18)
Enterococcus species
42 (14)
Klebsiella species
25 (8.4)
Proteus species
22 (7.4)
Enterobacter species
20 (6.7)
Streptococcus species
9 (3)
Citrobacter species
8 (2.7)
Staphylococcus aureus
7 (2.4)
NOTE. The number of isolates (360) exceeds the number of patients with CAUTI because some patients had
polymicrobial infection.
15
TABLE 3. General characteristics and in-ICU events potentially associated with mortality in cases and controls
Variable
Pa
Cases
Controls
(n = 273)
(n = 896)
45 36-57
44 34-57
.58
3 1-6
3 1-6
.85
1
127 (47)
452 (50)
2
130 (47)
366 (41)
3
16 (6)
78 (9)
Medical
167 (61)
527 (59)
Scheduled surgery
35 (13)
152 (17)
Unscheduled surgery
71 (26)
217
At ICU admission
SAPS II score, median IQR
LOD score, median IQR
Mc Cabe
.61
Admission category
.74
(24)
Transfer from ward
170 (63)
558 (64)
.79
Cardiac disease
50 (18)
150 (17)
.62
Respiratory Disease
60 (22)
174 (19)
.21
Renal Disease
6 (2)
29 (3)
.32
Liver Disease
16 (6)
44 (5)
.28
Immunodeficiency
34 (12)
98 (11)
.99
Uncomplicated diabetes mellitus
50 (18)
171 (19)
.16
Complicated diabetes mellitus
14 (5)
29 (3)
.28
Chronic coexisting conditions
Reason for ICU admission
16
Septic shock
38 (14)
156 (17)
.04
Cardiogenic shock
9 (3)
28 (3)
.67
Hemorragic shock
10 (4)
32 (4)
.99
Acute respiratory failure
80 (29)
262 (29)
.95
Acute exacerbation of COPD
15 (6)
40 (5)
.40
Acute renal failure
13 (5)
42 (5)
.95
Coma
54 (20)
131 (15)
.04
Trauma
4 (1)
11 (1)
.97
Multiple organ failure
20 (7)
39 (4)
.05
Other
30 (11)
155 (18)
.07
Catecholamine infusion
153 (56)
482 (54)
.84
Mechanical ventilation
12 (44)
314 (35)
.02
Use of antibiotics
197 (72)
688 (77)
.03
Use of broad-spectrum antibiotics
143 (52)
575 (64)
< .01
Extra-urinary sepsis
203 (74)
474 (53)
< .001
Antibiotic use b
198 (73)
701 (78)
.02
Shock or any organ failure
267 (98)
872 (97)
.80
First 48 hours in the ICU
Later during the ICU stay
NOTE. Data are expressed as number (%), unless otherwise indicated. IQR, interquartile range; SAPS II, Simplified
Acute Physiology Score version II; LOD, Logistic Organ Dysfunction; COPD, Chronic Obstructive Pulmonary
Disease.
a
b
Conditional logistic regression.
Antibiotics within 72 hours before the day CAUTI occurred (or before the corresponding day in controls).
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TABLE 4. Odds ratios (OR) of mortality associated with CAUTI
OR (95% CI)
Pa
ICU death
1.020 (0.796-1.306)
.88
Hospital death
1.185 (0.954-1.481)
.12
ICU death
0.846 (0.659-1.086)
.19
Hospital death
0.949 (0.763-1.181)
.64
Variable
Unadjusted analysis
Adjusted analysis
NOTE. ICU, intensive care unit.
a
Conditional logistic regression.
18
Appendix
Members of the Outcomerea study group:
Scientific committee:
Jean-François Timsit (Hôpital Albert Michallon and INSERM U823, Grenoble, France), Pierre Moine (Surgical
ICU, Denver, Colorado), Arnaud De Lassence (ICU, Hôpital Louis Mourier, Colombes, France), Elie Azoulay
(Medical ICU, Hôpital Saint Louis, Paris, France), Yves Cohen (ICU, Hôpital Avicenne, Bobigny, France), Maïté
Garrouste-Orgeas (ICU Hôpital Saint- Joseph, Paris, France), Lilia Soufir (ICU, Hôpital Saint-Joseph, Paris,
France), Jean-Ralph Zahar (Microbiology Department, Hôpital Necker, Paris, France), Christophe Adrie (ICU,
Hôpital Delafontaine, Saint Denis, France), Adel Benali (Microbiology and Infectious Diseases, Hôpital SaintJoseph, Paris France), Christophe Clec’h (ICU, Hôpital Avicenne, Bobigny, France), and Jean Carlet (ICU, Hôpital
Saint-Joseph, Paris, France).
Biostatistical and informatics expertise:
Jean-Francois Timsit (Group of Epidemiology, INSERM U578, Grenoble, France), Corinne Alberti (Medical
Computer Sciences and Biostatistics Department, Robert Debré, Paris, France), Muriel Tafflet (Outcomerea,
France); Frederik Lecorre (Supelec, France), and Didier Nakache (Conservatoire National des Arts et Métiers, Paris,
France).
Investigators of the Outcomerea database:
Christophe Adrie (ICU, Hôpital Delafontaine, Saint Denis, France), Caroline Bornstain (ICU, Hôpital de
Montfermeil, France), Alexandre Boyer (ICU, Hôpital Pellegrin, Bordeaux, France), Antoine Caubel (ICU, Hôpital
Saint-Joseph, Paris, France), Christine Cheval (SICU, Hôpital Saint-Joseph, Paris, France), Marie-Alliette Costa de
Beauregard (Nephrology, Hôpital Tenon, Paris, France), Jean-Pierre Colin (ICU, Hôpital de Dourdan, Dourdan,
France), Anne-Sylvie Dumenil (Hôpital Antoine Béclère, Clamart France), Adrien Descorps-Declere (Hôpital
Antoine Béclère, Clamart France), Jean-Philippe Fosse (ICU, Hôpital Avicenne, Bobigny, France), Samir Jamali
19
(ICU, Hôpital de Dourdan, Dourdan, France), Christian Laplace (ICU, Hôpital Kremlin-Bicêtre, Bicêtre, France),
Thierry Lazard (ICU, Hôpital de la Croix Saint-Simon, Paris, France), Eric Le Miere (ICU, Hôpital Louis Mourier,
Colombes, France), Laurent Montesino (ICU, Hôpital Bichat, Paris, France), Bruno Mourvillier (ICU, Hôpital
Bichat, France), Benoît Misset (ICU, Hôpital Saint-Joseph, Paris, France), Delphine Moreau (ICU, Hôpital SaintLouis, Paris, France), Etienne Pigné (ICU, Hôpital Louis Mourier, Colombes, France), Carole Schwebel (CHU A
Michallon, Grenoble, France), Gilles Troché (Hôpital Antoine, Béclère, Clamart France), Marie Thuong (ICU,
Hôpital Delafontaine, Saint Denis, France), Guillaume Thierry (ICU, Hôpital Saint-Louis, Paris, France), Dany
Toledano (CH Gonnesse, France), Eric Vantalon (SICU, Hôpital Saint-Joseph, Paris, France), and François Vincent
(ICU, Hôpital Avicenne, Bobigny, France).
20