Outcome in critically ill medical patients treated with renal replacement therapy for acute renal failure: comparison between patients with and those without haematological malignancies

Dominique D. Benoit1, Eric A. Hoste1, Pieter O. Depuydt1, Fritz C. Offner2, Norbert H. Lameire3, Koenraad H. Vandewoude1, Annemieke W. Dhondt3, Lucien A. Noens2 and Johan M. Decruyenaere1

Department of Internal Medicine, 1 Intensive Care Medicine, 2 Hematology and 3 Renal Divisions, Ghent University Hospital, 9000 Gent, Belgium

Correspondence and offprint requests to: Dominique Benoit, Medical Intensive Care Unit, 12K12IB, Ghent University Hospital, De Pintelaan 185, 9000 Gent, Belgium. E-mail: dominique.benoit{at}Ugent.be



   Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Background. Starting renal replacement therapy (RRT) for acute renal failure in critically ill patients with haematological malignancies is controversial because of the poor outcome and high costs. The aim of this study was to compare the outcome between critically ill medical patients with and without haematological malignancies who received RRT for acute renal failure.

Methods. We retrospectively collected data on all consecutive patients who received RRT for acute renal failure at the Medical Intensive Care Unit (ICU) of a University Hospital between 1997 and 2002, and assessed the impact of the presence of a haematological malignancy on the survival within 6 months after ICU admission by Cox proportional hazard models.

Results. Fifty of the 222 (22.5%) consecutive patients with haematological malignancies admitted to the ICU over the study period received RRT for acute renal failure compared with 248 of the 4293 (5.8%) patients without haematological malignancies (P< 0.001). Among patients who received RRT, those with haematological malignancies had higher crude ICU (79.6 vs 55.7%, P = 0.002) and in-hospital (83.7 vs 66.1%, P = 0.016) mortality rates, and a higher mortality at 6 months (86 vs 72%, P = 0.018) by Kaplan–Meier estimates compared with those without haematological malignancies. However, after adjustment for the severity of illness and the duration of hospitalization before ICU admission, haematological malignancy by itself was no longer associated with a higher risk of death (hazard ratio 1.04; 95% confidence interval, 0.73–1.54, P = 0.78).

Conclusions. Medical ICU patients with haematological malignancies have a higher rate of occurrence of acute renal failure treated with RRT and a higher mortality, compared with those without haematological malignancies. However, the presence of a haematological malignancy by itself is not a reason to withhold RRT in medical ICU patients with acute renal failure.

Keywords: acute renal failure; haematological malignancy; infection; intensive care unit; renal replacement therapy



   Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Acute renal failure requiring renal replacement therapy (RRT) is associated with a poor prognosis in patients with haematological malignancies [1–7]. Mortality rates of 80–90% have been reported in patients who underwent myeloablative allogeneic peripheral stem cell or bone marrow transplantation [2,3], increasing up to 85–100% in patients with haematological malignancies who require mechanical ventilation or who receive RRT in the context of multiple organ failure [4–7]. When RRT is required in an intensive care unit (ICU) setting, the mortality rates in patients with haematological malignancies consistently exceeded those observed in general ICU patients [8,9], a finding that could not be attributed solely to a more pronounced severity of illness [10,11]. In view of these results, and given the high costs, the severe emotional burden endured by these patients and their relatives, and the expected further decline in survival after hospital discharge [1,3], there are doubts about the appropriateness of RRT in this population [4,7]. However, the uncertainty over whether to provide RRT in critically ill patients with haematological malignancies is based essentially upon observations made before 1995 [4,5,10]. Due to a better selection of patients for referral to the ICU [12–14] and progress in supportive care [12–14], the mortality rates in critically ill patients with haematological malignancies have decreased over the past decade [12,13] approaching those observed in the general ICU population [13,14].

The aim of this study was to compare the outcome of critically ill patients with and without haematological malignancies who received RRT for acute renal failure between 1997 and 2002 at our centre, and to assess whether the presence of such a malignancy was independently associated with mortality within 6 months after ICU admission in this population.



   Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
This retrospective observational study was conducted at the Medical ICU of the Ghent University Hospital, a tertiary referral centre with 1060 beds. Patients admitted to this 14-bed ICU are at least 15 years old. This ICU is staffed by three intensive care physicians; two of them (D.D.B. and K.H.V.) have been trained in haemato-oncology. The medical management of patients with haematological malignancies is done in collaboration with the attending haematologists. Decisions regarding the indication for RRT, as well as the initial RRT modality, are made in agreement with the renal consultants. All consecutive patients admitted to this ICU between January 1997 and June 2002 who received RRT for acute renal failure were eligible for this study. Patients with a history of chronic renal failure requiring RTT before admission to the ICU or who were referred from the surgical or cardio-surgical ICU were excluded.

The following variables were collected retrospectively from charts and computerized databases: age, gender, duration of hospitalization before ICU admission, presence of haematological malignancy, Acute Physiology and Chronic Health Evaluation (APACHE) II score, need for mechanical ventilation and vasopressor therapy during admission, duration of mechanical ventilation, time from ICU admission to RRT, initial RRT modality (intermittent or continuous technique), length of stay at the ICU and outcome data, including vital status (alive or dead) at ICU and hospital discharge as well as vital status at 6 months and number of days of survival since ICU admission. The APACHE II score was calculated by using the worst values within the first 24 h of admission to the ICU. Patients for whom the Glasgow coma score was not available were considered to have a normal mental state. Predicted mortality rates calculated according to the APACHE II score and weighted by admission categories were also available. Mechanical ventilation included non-invasive and invasive modes. The use of vasopressors was defined as any vasopressor (epinephrine, norepinephrine, dopamine or vasopressin) or inotropic drug (dobutamine or milrinone) that was started during admission. At our ICU, the use of vasopressor and inotropic drugs is restricted to patients with persistent hypotension despite adequate volume replacement and inadequate cardiac output, or cardiac failure proven by pulmonary catheterization or echocardiography.

Additional information regarding patients with haematological malignancies was extracted from an existing MICU database [14] including type of haematological malignancy, disease status, use of intravenous chemotherapy within 3 weeks before ICU admission, allogeneic bone marrow transplantation, primary reason for admission to the ICU, do not resuscitate orders and time from ICU admission to the do not resuscitate orders. Based on previous observations [14–16] that the primary reason for admission to the ICU, and more particularly the presence of bacterial infection, may have a considerable impact on the outcome in this population, the primary diagnosis at admission in this database was assessed by an independent panel of three physicians blinded to the patient's outcome. This panel classified the patients according to the presence or absence of bacterial infection, the diagnostic certainty of infection (documented or clinically suspected) and the site of infection (pulmonary or non-pulmonary). The type of haematological malignancy was categorized into high grade malignancies including acute myelogenous leukaemia, acute lymphoblastic leukaemia and high grade non-Hodgkin lymphoma, and into low grade malignancies including all other types of haematological malignancies and aplastic anaemia. Active disease was defined as relapse or disease progression requiring chemotherapy or for which chemotherapy had been given within the 4 weeks prior to ICU admission. Hence, patients in complete or stable partial remission receiving consolidation chemotherapy were not considered to have active disease. This study was approved by the Ethical Committee of the Ghent University Hospital.

Statistical analysis
Continuous variables are expressed as median (interquartile range). Categorical variables are reported as counts and percentage. To assess differences between two independent groups, a Mann–Whitney U-test was used for continuous variables and a Fisher exact test for categorical variables. The major outcome variable in this study is mortality from any cause within the follow-up period of 6 months after admission to the ICU. Univariate and multivariate Cox proportional hazards models were used to assess the impact of the presence of a haematological malignancy on the outcome in this cohort of patients. We adjusted for the severity of illness (assessed by the APACHE II score), the duration of hospitalization before ICU admission and finally for all variables that were significantly different in the baseline characteristics between patients with and those without haematological malignancies, or related to the outcome in the univariate analysis at a P-level of 0.25, as well as those regarded as being clinically important (see Results). To avoid collinearity, only variables with a correlation of the estimates <0.6 were eligible for the final model. Stepwise elimination procedures were used. Event–rate curves were generated according to the method of Kaplan and Meier; comparison between survival probabilities of two groups was performed by a log-rank test. All reported P-values are two-tailed. When appropriate, hazard ratios (HRs) and 95% confidence intervals (95% CIs) are reported. All statistical analyses were carried out with SPSS 10 (SPSS Inc., Chicago, IL).



   Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Of the 4515 consecutive patients admitted to the medical ICU over a 4.5 year period, 298 (6.6%) received RRT for acute renal failure and 222 (4.9%) of the total population had a haematological malignancy. RRT for acute renal failure was instituted in 50 of the 222 (22.5%) patients with haematological malignancies, compared with 248 of the 4293 (5.8%) patients without haematological malignancies (P< 0.001). One patient with a haematological malignancy and 27 patients without haematological malignancies were excluded from further analysis because of missing data, resulting in a total of 270 acute renal failure patients who were treated with RRT available for analysis. The ICU mortality in patients without haematological malignancies excluded from the analysis was available in 22 of them and was comparable (11 out of 22, 50%) with the ICU mortality observed in those included in the analysis (see below). Twenty-one (7.7%) of the 221 patients without haematological malignancies were lost to follow-up and were censored in the survival analysis.

Differences in baseline characteristics, severity of illness and outcome between patients with and those without haematological malignancies (n = 270)
Patients with haematological malignancies were slightly younger (Table 1). They had a longer duration of hospitalization before ICU admission and were more severely ill compared with those without haematological malignancies, as indicated by the higher APACHE II score and predicted mortality rates, by the higher proportion of ventilated patients and by a more frequent use of continuous RRT (a modality preferentially used in patients with haemodynamic instability). The crude ICU and in-hospital mortality rates in patients with and those without haematological malignancies were 79.6 vs 55.7% (P = 0.002) and 83.7 vs 66.1% (P = 0.016), respectively. According to the Kaplan–Meier estimates (Figure 1), patients with haematological malignancies had a statistically significantly higher mortality at 6 months (86 vs 72%, P = 0.018) compared with those without haematological malignancies.


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Table 1. Baseline characteristics and severity of illness in medical ICU patients with and without haematological malignancies who received renal replacement therapy for acute renal failure (n = 270)a

 


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Fig. 1. Kaplan–Meier survival estimates in patients with (n = 49, solid line) and those without haematological malignancies who received RRT in the ICU (n = 221, interrupted line).

 
Impact of the presence of a haematological malignancy on the outcome in acute renal failure patients who received RRT at the medical ICU (n = 270)
The results of the univariate and multivariate survival analysis are shown in Table 2. By univariate survival analysis, haematological malignancy, duration of hospitalization before ICU admission, APACHE II score, need for ventilation and vasopressors during ICU stay, and the initiation of continuous RRT (compared with intermittent RRT) were all significantly related to a higher death rate. Except for continuous RRT which is started preferentially in patients with haemodynamic instability in our unit and which was not included in the multivariate analysis because of the risk of collinearity, all these variables were entered in a multivariate Cox's proportional hazard model. After adjusting for all these covariates, the presence of a haematological malignancy was no longer related to a higher death rate (HR 1.04; 95% CI 0.73–1.54, P = 0.78). Only the APACHE II score (HR 1.04; 95% CI 1.02–1.05, P<0.001), vasopressor use (HR 2.1; 95% CI 1.38–3.28, P = 0.001) and duration of hospitalization before admission to the ICU (HR 1.02; 95% CI 1.01–1.03, P<0.001) were significantly associated with a higher mortality within 6 months after ICU admission. In a bivariate analysis, the HR for haematological malignancy was 1.28 (95% CI 0.91–1.85, P = 0.16) after adjustment for the APACHE II score and 1.33 (95% CI 0.93–1.89, P = 0.12) after adjustment for the duration of hospitalization.


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Table 2. Impact of the presence of a haematological malignancy on the outcome in medical ICU patients with acute renal failure who received renal replacement therapy (n = 270)a

 
Impact of reason for admission, malignancy-related characteristics and severity of illness on the outcome in the subgroup of critically ill patients with haematological malignancies (n = 49)
Additional baseline characteristics, reasons for admission and in-hospital mortality rates in the subgroups of patients with haematological malignancies are shown in Table 3. Except for the admission diagnosis and mechanical ventilation, no other baseline characteristic was associated with in-hospital mortality. Patients with a proven or suspected bacterial infection had a trend to a lower in-hospital mortality compared with those with other complications precipitating ICU admission (20 out of 27, 74.1% vs 21 out of 22, 95.5%, respectively, P = 0.059). After adjustment for severity of illness (APACHE II score, ventilation and vasopressor use) and the duration of hospitalization before admission to the ICU, bacterial infection was independently related to a better survival within 6 months after ICU admission (HR 0.5; 95% CI 0.26–0.95, P = 0.03) compared with other complications. Only one patient with a non-bacterial complication precipitating ICU admission survived to hospital discharge. This patient was admitted to the ICU with an intra-cerebral bleeding and required RRT 2 weeks after admission to the ICU because of ventilator-associated pneumonia and sepsis. The only patient with active disease who survived to hospital discharge was admitted to the ICU because of bacterial infection. He died 99 days later from refractory haematological disease. We found no differences in do not resuscitate orders (six out of 27, 22.2 vs six out of 22, 27.3%, P = 0.75) between patients with and those without bacterial infection precipitating ICU admission. There was also no difference in median time from ICU admission to the do not resuscitate orders [11.5 days (9–16) vs 12.5 days (10–28.7), P = 0.59] and in length of stay at the ICU [8 days (2–25) vs 11.5 days (7–21), P = 0.76]. After 6 months, six of 27 (22.2%) patients with bacterial infection were still alive compared with one of 22 (4.5%) patients without bacterial infection (P = 0.11).


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Table 3. Malignancy-related characteristics, reasons for admission and in-hospital mortality rates in medical ICU patients with haematological malignancies who received RRT for acute renal failure (n = 49)

 


   Discussion
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
In this retrospective study, we found that patients with haematological malignancies more often required RRT for acute renal failure compared with those without haematological malignancies. In total, 22.5% of these patients required RRT during their ICU stay, compared with 5.8% of the general medical ICU patients. This is in accordance with a previous report in which patients with a past history of leukaemia or lymphoma had a >2-fold higher independent risk of developing acute renal failure compared with the general ICU population [11]. The higher incidence of acute renal failure in these patients is thought to be due to several factors, such as a higher susceptibility for infection, a more pronounced severity of illness, a more frequent use of nephrotoxic drugs such as amphotericin B, aminoglycosides, cis-platinum and cyclosporin A, and specific bone marrow transplantation-related syndromes such as veno-occlusive disease or haemolytic–uraemic syndrome [1,2,3,6].

The presence of a haematological malignancy was clearly associated with a lower survival in this cohort of acute renal failure patients who received RRT. As shown in Figure 1, patients with haematological malignancies had a 6 months survival probability of only 14% compared with 28% in those without haematological malignancies (P = 0.018). This difference in probability of survival is due predominantly to a higher death rate during the first weeks of admission in patients with haematological malignancies and less to a further decline in survival after hospital discharge. This can be attributed to a more pronounced severity of illness upon admission to the ICU. Patients with haematological malignancies, who had higher APACHE II scores, higher APACHE II expected mortality rates, required mechanical ventilation more often during ICU admission and continuous modalities of RRT, were also initiated more often compared with those without haematological malignancies. They also had a longer duration of hospitalization before admission. However, after adjusting for these confounding variables, we found that the presence of a haematological malignancy was no longer associated with a higher risk of death within 6 months after ICU admission. This finding is in contrast to a recent report [11]. However, in this previous report [11], the authors did not adjust for the duration of hospitalization before ICU admission, an important prognostic indicator of adverse outcome in critically ill patients with haematological malignancies and solid tumours [17]. A previous hospitalization is also known to be adversely related to the outcome in general ICU patients with acute renal failure [8,18]. In our study, the duration of hospitalization before admission to the ICU was a stronger predictor of poor outcome than the presence of a haematological malignancy. Moreover, de Mendonça et al. [11] used 30-day mortality as the end-point rather than 6 months mortality as in our study, hence they did not account for the further decline in survival rate after this period of time in patients without haematological malignancies. Finally, de Mendonça et al. [11] analysed the impact of a past history of a haematological malignancy on the outcome in a mixed ICU population of medical and surgical patients. As on one hand, patients with haematological malignancies are more often referred to the ICU with medical complications, and, on the other, surgical patients requiring RRT have lower mortality rates [9], the effect of the underlying haematological malignancy on the outcome may have been overestimated in their study.

Our results indicate that the presence of a haematological malignancy by itself is not a reason to withhold RRT in critically ill medical patients with acute renal failure. However, given the low crude survival probability of only 14% at 6 months, this does not imply that every patient with a haematological malignancy should be offered RRT. Once discharged from the ICU, the mortality rate in patients with haematological malignancies remained nearly constant over the 6 months follow-up period. This can only be explained by a good selection of patients with regard to the underlying haematological disease status and subsequent long-term outcome, and by the fact that the majority of the patients who received RRT despite active (but potentially curable) haematological disease died during their ICU stay. Only one out of 10 patients with active disease who received RRT survived to hospital discharge but died 80 days after ICU admission because of refractory disease. Therefore, the underlying disease status and subsequent estimated long-term outcome and quality of life, as in every general ICU patient, should be taken into account before starting RRT in patients with haematological malignancies. Moreover, based on our results, it seems that among severely ill patients with haematological malignancies, those with proven or presumed bacterial infection precipitating ICU admission might be the best potential candidates to receive an RRT trial. These patients had an in-hospital mortality of 74.1%, which is similar to general ICU patients with sepsis requiring RRT. Neveu et al. [18] reported in general ICU patients who received RRT for acute renal failure in-hospital mortality rates of 70.8% in those with septic syndrome and 79.4% in those with septic shock. In a more recent study, Metnitz et al. [9] reported a mortality of 67.3 and 73.9%, respectively. In contrast, mortality in patients with non-bacterial complications precipitating ICU admission in our study was as high as 95.5%.

The better outcome in patients with bacterial infection is somewhat surprising but has already been observed in a general population of critically ill patients with haematological malignancies [14] as well as in bone marrow transplant recipients [15,16]. This finding can be explained by an improvement in supportive care and management of septic shock over the past decade in general and in patients with haematological malignancies in particular [12–14] and by the increasing referral of patients with severe and often irreversible non-bacterial complications to the ICU. In contrast to the study of Lanore et al. [5], no patient had a rapidly reversible non-bacterial complication such as hypercalcaemia, severe electrolyte disorders associated with cell lysis syndrome or toxic nephropathy in our study. Six patients had a transplant-related hepatic toxicity, veno-occlusive disease or haemolytic–uraemic syndrome for which no effective therapy is available [2,3]. Hepatic failure and/or veno-occlusive disease secondary to high dose regimens is the strongest predictor of severe renal failure in bone marrow transplant recipients and is associated with the highest mortality [2,3,6]. In a study by Gruss et al. [2], only one out of 11 patients with veno-occlusive disease and RRT requirement survived, while Hahn et al. [3] reported that none of the 18 patients with veno-occlusive or graft-versus-host disease requiring RRT were long-term survivors. Another four of our patients had fungal, viral or parasitic infections which remain difficult to treat and still carry high mortality rates in patients with haematological malignancies [19], particularly in an ICU setting [20]. Another eight patients with cardiac complications did not survive to hospital discharge because none of them could receive effective anti-platelet or anti-coagulation therapy because of thrombocytopenia. In addition, neither coronary bypass nor valve replacement surgery was proposed in these patients because of an uncertain prognosis. Therefore, it is acceptable not to offer RRT to critically ill patients with haematological malignancies and acute renal failure due to severe complications other than bacterial infection.

Our study has a number of limitations. Unfortunately, given the retrospective observational design of this study, we do not have data regarding patients who were not referred to the ICU and/or who did not receive RRT because of end-of-life decisions. Therefore, we cannot exclude that the absence of difference in outcome between the two populations after adjustment for confounding variables is due to selection bias. Nevertheless, our results reflect the admission and treatment policy of a tertiary university referral centre and indicate that RRT in acute renal failure medical ICU patients with haematological malignancies cannot be considered to be futile, particularly in the subset of patients with documented or clinically suspected bacterial infections precipitating ICU admission. We cannot also rule out that a certain number of patients with haematological malignancies were misclassified with regard to their admission diagnosis. However, the main admission diagnosis in patients with haematological malignancies was assessed by an independent panel of physicians blinded to the patient's outcome in order to minimize this potential problem. By doing so, bias related to the preferential categorization of the patients by the main investigator could also be excluded. The observation that patients with documented and clinically suspected bacterial infections had comparable mortality rates also indicates that this was not a substantial problem (Table 3).

In conclusion, medical ICU patients with haematological malignancies have a higher rate of occurrence of acute renal failure treated with RRT and a higher mortality compared with medical ICU patients without these malignancies. However, the presence of a haematological malignancy by itself is not a reason to withhold RRT in medical ICU patients with acute renal failure.



   Acknowledgments
 
We are indebted to Sabine Vandemoortele for helping to collect the data. Part of this work was presented at the 24th International Symposium on Intensive Care and Emergency Medicine Annual Meeting in Brussels, Belgium, March 30–April 2, 2004.

Conflict of interest statement. None declared.



   References
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 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 

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Received for publication: 24. 8.04
Accepted in revised form: 10.11.04





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