Sequential organ failure predicts mortality of patients with a haematological

Copyright Blackwell Munksgaard 2005
Eur J Haematol 2005: 74: 511–516
All rights reserved
EUROPEAN
JOURNAL OF HAEMATOLOGY
Sequential organ failure predicts mortality
of patients with a haematological
malignancy needing intensive care
Cornet AD, Issa AI, van de Loosdrecht AA, Ossenkoppele GJ, Strack
van Schijndel RJM, Groeneveld ABJ. Sequential organ failure predicts
mortality of patients with a haematological malignancy needing
intensive care.
Eur J Haematol 2005: 74: 511–516. Blackwell Munksgaard 2005.
Alexander D. Cornet1, Aart I. Issa1,
Arjan A. van de Loosdrecht2,
Gert J. Ossenkoppele2,
Rob J. M. Strack van Schijndel1,
A. B. Johan Groeneveld1
1
Abstract: Objectives: Poor survival of patients with a haematological
malignancy admitted to the intensive care unit (ICU) prompts for
proper admission triage and prediction of ICU treatment failure and
long-term mortality. We therefore tried to find predictors of the latter
outcomes. Methods: A retrospective analysis of charts and a prospective follow-up study were done, of haemato-oncological patients,
admitted to our ICU in a 7-year period with a follow-up until 2 yr
thereafter. Clinical parameters during the first four consecutive days
were taken to calculate the simplified acute physiology (SAPS II) and the
sequential organ failure assessment (SOFA) scores, of proven predictive
value in general ICU populations. Results: From a total of 58 patients
(n ¼ 47 with acute myelogenous leukaemia or non-Hodgkin lymphoma), admitted into ICU mostly because of respiratory insufficiency,
sepsis, shock or combinations, 36 patients had died during their stay in
the ICU. Of ICU survivors (n ¼ 22), 20 patients died during follow-up
so that the 1-year survival rate was only 12%. The SAPS II and particularly the SOFA scores were of high predictive value for ICU and
long-term mortality. Conclusions: Patients with life-threatening complications of haematological malignancy admitted to ICU ran a high
risk for death in the ICU and on the long-term, and the risk can be well
predicted by SOFA. The latter may help us to decide on intensive care in
individual cases, in order to avoid potentially futile care for patients with
a SOFA score of 15 or higher.
Patients admitted into the intensive care unit (ICU)
because of complications in the treatment of a
haematological malignancy often have a poor
prognosis, with an ICU or hospital mortality rate
of 50–95%. The outcome varies widely among
studies, however, partly due to differences in casemix, with extremely poor outcomes, for instance,
reported for bone marrow/stem cell recipients
(1–12). Moreover, the prognosis of haemato-oncological patients on the ICU might have improved
over the past decades, at least on the short term (9,
11, 12). Data on long-term mortality (up to 1 yr)
are scarce, however, so that it cannot be fully
assessed if the efforts in the ICU are still ÔworthwileÕ
(3, 7, 8, 13). Indeed, long-term survival may depend
Department of Intensive Care, Institute for
Cardiovascular Research, Vrije Universiteit Medical
Centre, Amsterdam, the Netherlands; 2Department of
Haematology, Vrije Universiteit Medical Centre,
Amsterdam, the Netherlands
Key words: haematological malignancy; ICU (Intensive
Care Unit); SOFA-score; SAPS II; long-term survival
Correspondence: Prof. Dr Johan Groeneveld MD PhD
FCCP FCCM, Intensive Care, Vumc, De Boelelaan 1117
1081 HV, Amsterdam, the Netherlands
Tel.: +31-20-4444178
Fax: +31-20-4442392
e-mail: [email protected]
Accepted for publication 19 December 2004
on the prognosis of the underlying disease rather
than on superimposed vital organ dysfunction
necessitating intensive care, while the latter may
be of greater importance in predicting short-term
mortality (6–8, 11, 13).
Prediction of intensive care treatment failure or
success and long-term outcome is important to help
decision-making concerning ICU admission once a
life-threatening complication of haematological
malignancy has developed. In the past, several
scoring methods have been developed to predict
whether or not general ICU patients will survive.
Even though some of these systems take the
presence of haematological malignancy into
account, it is unclear if the Acute Physiology and
511
Cornet et al.
Chronic Health Evaluation (APACHE II/III) score
(2, 5, 6, 8–10, 12), the Simplified Acute Physiology
Score (SAPS II) (3, 7, 8, 10, 14) and the Sequential
Organ Failure Assessment (SOFA) (11) are of
major value in predicting ICU survival from such
malignancies. Surprisingly, no or only minimal
predictive values in haemato-oncologic patients
have been reported (4–8, 10, 12, 14).
The current study was undertaken to evaluate the
ICU and long-term (i.e. 1 and 3 yr) outcome and its
potential predictors SAPS II and SOFA, for
critically ill patients with a haematological malignancy.
Patients and methods
A retrospective study was done on consecutive
patients admitted with a known haematological
malignancy from the haematological department
into the 7-bed medical ICU of our 700-bed university hospital, from 1 November 1995 to 31 December 2002. Follow-up was completed on 1 January
2004, and for only one, ultimately dying patient the
survival time remained unknown. Predefined lists
were completed of data collected, in a standardized
manner, from patient charts.
Demographics,
underlying
haematological
malignancy, reason of admission to the ICU, and
comorbidity were taken from the charts. Patients
had been monitored by repeated laboratory determinations, at least once daily, and, when necessary,
by invasive haemodynamic and ventilatory monitoring, and data had been recorded in an electronic
patient data management system in use in our ICU.
Data were extracted from the electronic and written
patient charts in order to calculate, using the worst
value in a 24 h time frame for each variable, and for
the day of admission (Day 0) as well as the three
following days (Days 1–3), the Simplified Acute
Physiology Score (SAPS II, 0–160) (15), that takes
the presence of a haematological malignancy into
account, and the Sequental Organ Failure Assessment (SOFA, 0–24) score (Table 1, Ref. 16). The
former score takes age, type of admission, presence
of chronic disease and 12 organ-specific clinical and
laboratory variables into account and the latter
consists of a score of six organ-specific clinical and
laboratory variables. The presedation score on the
Glasgow coma scale was used. While SAPS II is
typically an admission score, the daily SOFA has
been developed to characterize disease course in
time. Daily chest radiographs were scored from 1 to
4 for the number of quadrants with alveolar
consolidations and together with ventilatory and
gas exchange parameters, the Lung Injury Score
(LIS, 17) was calculated. The score ranges between
0 and 4 and a value >2.5 have been regarded to
indicate acute respiratory distress syndrome
(ARDS). For scoring systems, missing values were
classified as normal. Likely clinical infection
sources were noted, as well as microbiological
results, including those obtained from bronchoalveolar lavage (BAL) fluid, within a window of 7 d
around the day of admission. The use and duration
of inotropic support, mechanical ventilation and
continuous renal replacement techniques were
recorded.
Statistical analyses
Outcome groups defined on the basis of mortality/
survival in the ICU were compared with help of an
unpaired Mann–Whitney U-test or, for categorical
variables with the Fisher’s exact and v2-tests. The
log rank test was used to compare long-term
mortality in SOFA strata, after constructing
Kaplan–Meier survival plots. Receiver operating
characteristic (ROC) curves were constructed, plotting sensitivity vs. 1-specificity to evaluate the
predictive value of variables for ICU outcome
and the more an area under the curve (AUC with
95% confidence intervals, CI) approaches 1, the
Table 1. The sequential organ failure assessment (SOFA) score
SOFA
0
1
£400
2
£300
3
£200
4
PaO2/FiO2
>400
Platelets (·109/L)
Bilirubin (lM/L)
No Hypotension
Glasgow coma score
Scale
Creatinine (lMol/L)
Urinary output (mL/d)
>150
<20
£150
20–32
MAP <70
£100
33–101
Dop £5 or Dob (any dose)
£50
102–204
Dop >5, Epi £0.1 or Nor £ 0.1
£100
With respiratory support
£20
>204
Dob >15, Epi >0.1 or Nor >0.1
15
>170
13–14
110–170
10–12
171–299
6–9
300–440
<500
<6
>440
<200
PaO2: partial pressure of O2 in arterial blood; FiO2: inspiratory O2 fraction; MAP: mean arterial pressure, mmHg; Nor: norepinephrine; Dob: dobutamine; Dop: dopamine; Epi:
epinephrine, adrenergic agents administered for at least 1 h (in lg/kg/min).
512
Sequential organ failure predicts mortality of patients
greater the predictive value. Data were summarized
by mean ± standard deviation (SD) or median
(range), the latter for survival times. A P-value
< 0.05 was considered statistically significant.
Results
Patient characteristics
In Table 2, the demographics are shown. The most
frequent reason for admission was respiratory
insufficiency, followed by pneumonia, renal insufficiency, shock and sepsis. Ninety percent (52/58) of
the patients had undergone intubation and mechanical ventilation, shortly after admission, while one
patient received non-invasive ventilation in the
ICU.
ICU outcome and its determinants
Sixty-two percent (36/58) patients died during their
stay in the ICU, and there was no change from
1995 to 2002. None of the reasons for admission
was associated with an increased mortality on the
ICU. The median length of stay of ICU nonsurvivors was 7.5 (0–48) d. Table 3 describes other
Table 2. Patient characteristics
Age (yr)
Men/women
In-hospital days before ICU
Time from haematological diagnosis (wk)
Acute myelogenous leukaemia
Chronic myelogenous leukaemia
Chronic lymphatic leukaemia
Hodgkin's disease
Non-Hodgkin lymphoma
Multiple myeloma
Allogeneic stem cell transplantation
Autologous stem cell transplantation
Prior radiotherapy
Day 1 last chemotherapy, <4 wk
No chemotherapy
Complete remission
Partial remission
Reason for admission
Infection/sepsis
Shock
PostCPR
Respiratory insufficiency
Renal insufficiency
Myocardial infarction
Liver insufficiency
Postoperative
Survival duration, days from admission
Length of stay in the ICU, d
Mortality during follow up
ICU non-survivors
(n ¼ 36)
ICU survivors
(n ¼ 22)
53.1 € 14.4
20/16
14 € 13
98 € 171
12 (33)
1 (28)
1 (28)
1 (28)
16 (44)
5 (14)
4 (11)
10 (28)
4 (11)
17 (47)
7 (19)
12 (33)
7 (19)
54.1 € 16.2
12/10
18 € 15
82 € 163
8 (36)
9 (25)
7 (19)
2 (5)
12 (33)
7 (19)
1 (3)
1 (3)
2 (5)
9 € 10
9 € 10
11
3
1
3
4
15
5
6
3
(50)
(14)
(4)
(14)
(18)
(68)
(23)
(27)
(14)
2
1
2
5
1
(9)
(5)
(9)
(22)
(4)
3 (14)
406 € 431
22 € 31
20 (91)
Mean € SD or number (percentage), where appropriate. ICU: intensive care unit;
CPR: cardiopulmonary resuscitation.
Table 3. Variables on the day of admission
ICU non-survivors
(n ¼ 36)
Hemodynamics
Heart rate (min)
Systolic blood pressure (mm Hg)
Mean arterial blood pressure (mm Hg)
Use of inotropic agents
Respiration
Duration (d)
PaO2, (mm Hg)
FiO2
PaO2/FiO2
PEEP (cm H2O)
Total respiratory compliance (mL/cm H2O)
Lung injury score
Renal function
Renal replacement therapy within 4 d
Urinary output (mL/d)
Serum creatinine (lmol/L)
Serum urea (mmol/L)
Hematology
Haematocrit (%)
White blood cell count (·109/L)
Leucocytopenia <1 (·109/L)
Prior duration leucocytopenia (d)
Platelets (·109/L)
Thrombocytopoenia <100 (·109/L)
Prothrombin time, international ratio
Activated partial thromboplastin time (s)
Neurology
Glasgow coma scale
Infection
Body temperature ( C)
Documented respiratory infection
Bacteremia (within 7 d window)
Use of antibiotics (within 7 d window)
Blood biochemistry
Sodium (mmol/L)
Potassium (mmol/L)
Bicarbonate (mmol/L)
Bilirubin (lmol/L)
Albumin (g/L)
Glucose (mmol/L)
Lactate dehydrogenase (U/L)
ICU survivors
(n ¼ 22)
132 € 39
96 € 28
66 € 19
25 (69)
123 € 38
116 € 47
78 € 33
11 (50)
9
80
78
114
8
29
2.5
18
85
69
144
8
36
2.2
€
€
€
€
€
€
€
7
41
21
67
3
12
0.7
€
€
€
€
€
€
€
25
40
21
90
4
14
0.9
5 (13)
1555 € 1579
170 € 101
17 € 10
4 (18)
1766 € 1335
208 € 223
20 € 14
25 € 8
7.2 € 10.1
14 (39)
3€5
50 € 66
32 (89)
1.62 € 0.35
52 € 40
29 € 5
8.0 € 8.5
4 (18)
3€6
110 € 146*
14 (64)*
1.45 € 0.41*
46 € 22
13 € 2
12 € 3
37.9 € 1.8
6 (17)
21 (58)
26 (72)
38.0 € 1.7
144
4.2
19.5
65
20
9.5
1030
142
4.0
22.5
18
20
8.9
1081
€
€
€
€
€
€
€
8
1.0
5.7
70
7
4.5
1142
16 (73)
17 (77)
€
€
€
€
€
€
€
7
1.1
4.6
16**
6
4.3
990
Mean € SD or number (percentage), where appropriate. PaO2: partial pressure of O2
in arterial blood; FiO2: inspiratory O2 fraction.
*P < 0.05.
**P < 0.01.
characteristics of survivors and non-survivors and
shows the prognostic significance of thrombocytopenia, prolonged clotting times and hyperbilirubinaemia, rather than underlying disease. The
frequency and severity of leucocytopenia on admission and its course over the subsequent 3 d did not
have prognostic significance. Nevertheless, the Day
0 SOFA scores differed between leucocytopenic and
non-leucocytopenic patients (P < 0.001), with
values for the SOFA-score of 11.8 ± 3.1 (with
leucocytopenia) and 8.4 ± 3.7 (without leucocytopenia). The Day 0 SOFA score also differed
between thrombocytopenic and non-thrombocytopenic patients (P < 0.001). Bronchoalveolar lavage
513
Cornet et al.
Scoring systems
The Day 0 SAPS II was higher (P < 0.01) in ICU
non-survivors (58 ± 17) than in survivors
(46 ± 14). Table 4 and Fig. 1 show the prognostic
significance of the SOFA score for ICU mortality.
The AUC for the ROC curve for Day 0 SOFA was
Table 4. SOFA-score and outcome
SOFA on day
0
1
2
3
ICU n
58
55
47
43
ICU non-survivors
10.6
11.2
10.7
11.1
€
€
€
€
ICU Survivors
3.7
3.7
4.0
4.0
6.7
6.9
6.3
7.6
€
€
€
€
3.4
3.4
3.6
3.9
P
<0.001
<0.001
<0.001
<0.01
SOFA: sequential organ failure assessment. ICU: intensive care unit.
30
Died
Number of patients
Survived
20
10
0
0.8
0.6
SOFA
15–20
0.4
10–15
5–10
0.2
0–5
0.0
0
200
400
600
Days
800
1000 1200
1400
Fig. 2. Kaplan–Meier plot of long-term survival, in the
strata (Fig. 1) of Day 0 SOFA (log rank test: P < 0.001).
SOFA 0–5, n ¼ 10; SOFA 5–10, n ¼ 27; SOFA 1–15, n ¼
16; SOFA 15–20, n ¼ 5.
0.77 (95% CI 0.65–0.90, P < 0.001) and for the
SAPS II score 0.70 (95% CI 0.56–0.84, P < 0.01).
The maximum (during the first 4 d of ICU stay)
SOFA was 12.8 ± 3.5 in non-survivors and
8.1 ± 3.8 in survivors (P < 0.001) and the AUC
under the ROC curve was 0.80 (95% CI 0.69–0.91,
P < 0.001). The mean SOFA score, over the first
4 d of ICU, was 6.4 ± 3.3 in survivors and
11.2 ± 3.5 in non-survivors (P < 0.001), with an
AUC under the ROC curve for mortality prediction
of 0.84 (95% CI 0.74–0.94, P < 0.001).
Long-term outcome
The median survival time of ICU survivors was 307
(range 6–1417) days after admission or 254 (0–
1400) days after ICU discharge, because 20 patients
had died after discharge from the ICU during time
to follow-up (Fig. 2). The 22 ICU survivors had a
length of stay in the ICU of median 7 (1–117) days.
The two long-term survivors until follow-up ended
had a non-Hodgkin lymphoma as underlying
disease. The overall 1-yr survival rate was 12%
and the 3-yr survival 5%. For ICU survivors, the
1-yr survival rate was 33%, with a median survival
time for ultimate non-survivors of 258 (6–1417)
days. The SOFA score was a determinant of
survival time (Fig. 2).
Discussion
0–5
5–10
10–15
15–20
SOFA
Fig. 1. Sequential organ failure assessment (SOFA) scores
and ICU survival (P < 0.01). ICU mortality increases from
20% at Day 0 SOFA 0–5, 63% at SOFA 5–10, 75% at
SOFA 10–15 to 100% at SOFA 15–20 points.
514
1.0
Survival
(BAL) was performed (within a 7 d window) in 17
patients and microorganisms were found in 8, but
there was no difference among outcome groups.
Aspergillus fumigatus was recovered in BAL from
two patients ultimately dying in the ICU. Tracheal
aspirate cultures were positive in 19 patients,
without prognostic significance. Another patient
with A. fumigatus in tracheal aspirate survived the
ICU stay. Thirteen patients had a prior autologous
stem cell transplantation, they all died within the
follow-up period, 6–2798 d after their transplantation. Five patients had undergone allogeneic stem
cell transplantation and they had died also within
the follow-up period, even though one patient lived
for 790 d after ICU admission. In any case, 13/17
patients with stem cell transplants had died in the
ICU.
Our study shows that the prognosis for patients
who are admitted to the ICU, having a haematological malignancy, is dismal, particularly on the
long term, and that the ICU outcome and survival
time can be well predicted by SOFA.
Sequential organ failure predicts mortality of patients
The overall ICU and hospital mortality of
haemato-oncologic patients reported in the literature varies between 50% and 95% (1–12), so that
our persistently high ICU mortality rate of about
60% may not indicate substantial improvement
over time, while greatly exceeding the almost 27%
mortality in our unit for general critically ill
patients (18). Age was not a prognosticator, in
contrast to other reports (5, 9, 12). Our results, as
those collected by others (12), also do not confirm
that (prolonged) mechanical ventilation is associated with a very poor outcome (1, 4–6, 10), since
respiratory insufficiency was a major reason for
ICU admission in our patients and most of them
had been intubated and mechanically ventilated
from the day of admission on. In contrast, other
investigators noted that the combination of
mechanical ventilation and (need for) renal replacement therapy in haematological malignancy almost
precluded survival (3, 6–8, 10), while this was not
the case in our study. The same applies for the poor
treatment status of the underlying malignancy
(leukaemia), postbone marrow transplantation,
leucocytopenia, septic shock and need for inotropes, carrying an adverse prognosis in some
studies (2, 3, 5, 7, 9–11), while these factors,
including the type of underlying malignancy, the
type and intensity of prior treatment and (duration
of) leucocytopenia were no major determinants of
ICU outcome in our study, in accordance with
recent literature (6, 19). Univariate predictors of
mortality in our series included thrombocytopenia
and elevated clotting times, as reported before (10).
Leuco- and thrombocytopenia related to organ
dysfunction (SOFA), possibly via toxicity of prior
chemotherapy or superimposed infection/sepsis,
suggesting a role of cytopenia in organ dysfunction.
The prolonged clotting times may relate to disseminated intravascular coagulation, in the presence of
similar albumin levels suggesting similar hepatic
protein synthesis, even in the presence of hyperbilirubinaemia. The prognostic importance of liver
abnormalities has been rarely reported before (6,
10). We can only speculate on the role of disseminated intravascular coagulation in a dismal outcome.
Nevertheless, the outcome of our patients was
relatively hard to predict by single variables, and
the observation that SOFA was a better predictor
than individual variables may conform with other
studies (16). The high predictive value of the SOFA
score underscores the use of organ-oriented scoring
systems in haemato-oncological, critically ill patients to judge prognosis (3, 6, 8, 10), even though
Blot et al. (14) reported lack of predictive value of
organ dysfunction scoring on outcome of haematooncological disease in the ICU. The discrepancy
with our study can be explained by the design of the
Blot et al. (14) study, enrolling patients in the
haematological wards only, while the scoring systems have been developed for ICU patients. Our
data thus suggest that SOFA better predicts than
admission disease severity scores such as the
APACHE II/III or the SAPS II scores, that may
not predict well in haemato-oncological patients (3,
5, 6, 8, 11, 12, 14). Indeed, the mean and maximum
SOFA scores performed even better than the Day 0
SOFA score in our patients, as suggested before for
a general ICU population (16). The ICU mortality
for the latter populations approaches 20% at
SOFA 6–7 until 80% at SOFA of 11 or higher
(16). The data also suggest that mortality at low
and intermediate SOFA scores is higher in haemato-oncological than in non-haemato-oncological,
critically ill patients, but apparently this does not
limit the predictive value of the SOFA score. In
contrast, mortality has been reported to be higher
for haemato-oncological than for non-haematooncological patients at low and intermediate disease severity scores, such as the SAPS II score, and
this may have contributed to a relatively poor
predictive value in the former patients (2, 4, 14).
Inclusion of platelet counts, having predictive
value, in the SOFA and not in the SAPS II score
may have contributed to greater predictive value of
the former.
Our study confirms the prognostic value of the
SOFA score in critical haemato-oncologic disease,
in a single prior publication on the subject, on 30
patients in a Scandinavian ICU (11) and extends
these observations regarding its relation with longterm outcome. It suggests that a haemato-oncological patient, who is admitted with a SOFA score of
15 or higher will not survive an ICU stay. Obviously, we only studied a small population, so that
treatment withdrawal in a patient with SOFA of 15
or higher cannot be defended on the basis of our
study alone. Even though 38% of our patients left
the ICU alive, the overall long-term prognosis is
still grim, with a 1-yr survival of only 12%, again
well predicted by the SOFA score on ICU admission and relatively independent of (the prognosis
of) underlying haemato-oncological disease. The
latter observation contrasts with studies by Yau
et al. (13) and Massion et al. (8), in which the longterm prognosis was primarily determined by that of
the haematological malignancy rather than by
organ dysfunction, but agrees with observations
by Kroschinsky et al. (7). The 1-yr survival was
about 20% in the Kroschinsky et al. (7) and Silfvast
et al. (11) studies, and 13% in the Yau et al. (13)
studies, and the 1-yr survival of our ICU survivors
of 33% also agrees with the literature (2, 3, 13). Our
results are finally in agreement with the predictive
515
Cornet et al.
value of SAPS II and particularly of SOFA for
outcome after ICU discharge of general critically ill
patients (20).
Summarizing, our current data, particularly
when confirmed prospectively in a larger population, may help to decide on intensive care for
individual critically ill patients with a haematological malignancy, in order to avoid potentially futile
care for those with a SOFA score of 15 or higher.
10.
11.
12.
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