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(Chest. 2004;126:1604-1611.)
© 2004 American College of Chest Physicians

Outcome and Prognostic Factors of Hematopoietic Stem Cell Transplantation Recipients Admitted to a Medical ICU*

Ayman O. Soubani, MBBS, FCCP; Eiad Kseibi, MD; Joseph J. Bander, MD; Jared L. Klein, MD; Geeta Khanchandani, MD; Huma P. Ahmed, MD and Jorge A. Guzman, MD

* From the Division of Pulmonary, Critical Care, and Sleep Medicine (Drs. Soubani, Kseibi, Bander, Khanchandani, Ahmed, and Guzman), and Stem Cell Transplantation Section (Dr. Klein), Wayne State University School of Medicine, Detroit, MI.

Correspondence to: Ayman O. Soubani, MBBS, FCCP, Harper University Hospital, Division of Pulmonary, Critical Care and Sleep Medicine, 3990 John R- 3 Hudson, Detroit, MI 48201; e-mail: asoubani{at}med.wayne.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Objective: To assess the outcome of adult hematopoietic stem cell transplantation (HSCT) recipients who were admitted to a medical ICU (MICU), and to identify the measurable predictors of their MICU outcome.

Design: Retrospective chart review study.

Setting: MICU in a tertiary care, university-affiliated medical center with a comprehensive cancer program.

Patients: Consecutive adult HSCT recipients admitted to the MICU between January 1998 and June 2001.

Measurements and main results: Eighty-five patients were admitted to the MICU, representing 11.4% of patients who had undergone HSCT during the study period. The mean (± SD) age at MICU admission was 46.6 ± 11.4 years (women, 67%; men, 33%). Forty-five patients (53%) underwent allogeneic HSCT, and 40 patients (47%) underwent autologous HSCT. Fifty-one patients (60%) required mechanical ventilation (MV). Fifty-two patients (61%) survived their MICU stay, and 35 patients (41%) were discharged alive from the hospital. The long-term survival rate (ie, > 6 months) in this cohort was 28%. Nineteen mechanically ventilated patients (37%) survived their MICU stay, and 33 patients (97%) survived who did not require MV (p < 0.01). The independent predictors of poor outcome during the MICU stay were elevated serum lactate level on admission to the MICU, the need for MV, and the presence of more than two organ systems that failed.

Conclusions: The study showed short-term and long-term survival rates among adult HSCT recipients who had been admitted to MICU that were higher than those previously reported. While there were no absolute predictors of mortality, patients with higher MICU admission serum lactate levels, those requiring MV, or those developing more than two organ system failures had poor MICU outcomes.

Key Words: bone marrow transplantation • complications • hematopoietic stem cell transplantation • mechanical ventilation • medical ICU • multiorgan system failure • outcome • prognosis


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Hematopoietic stem cell transplantation (HSCT) with stem cells harvested either from peripheral blood or marrow is now the standard of treatment for a variety of malignancies.123 Complications associated with HSCT are significant, and result in heightened morbidity and mortality. These complications are due to drug toxicities and immunosuppression from conditioning regimens, infections, bleeding, graft-vs-host disease (GVHD), and relapse of the original disease. It is estimated that 25 to 40% of HSCT recipients are admitted to the medical ICU (MICU) for the management of these complications.456789 Previous studies45671011121314 have shown that the outcome of patients who are admitted to the MICU, especially those requiring mechanical ventilation (MV), is very poor. Consequently, some clinicians have questioned the utilization of mechanical ventilatory support for these patients as a futile intervention. As a result, attempts were also made to identify the predictors of MICU outcome in HSCT recipients, however, these studies45678910111213141516171819202122 showed conflicting results.

Although the survival rate of HSCT recipients admitted to the MICU has been steadily improving, it remains at < 45%, with a long-term survival rate of < 20%.1521 This study was conducted to analyze the clinical characteristics and survival rates of HSCT recipients who had been admitted to the MICU, including those who required MV, and to identify the predictors of adverse MICU outcomes.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Karmanos Cancer Institute is a comprehensive cancer center with a busy stem cell transplantation service. Patients are cared for in a specialized unit, however, this unit does not have critical care beds. If a patient’s condition deteriorates, that patient is transferred to the MICU. The criteria for admission to and discharge from our MICU follow the guidelines set by the American College of Critical Care Medicine and Society of Critical Care Medicine.23 The MICU is managed by full-time faculty members of the Pulmonary and Critical Care Division, and, in the case of HSCT recipients, there is involvement by bone marrow transplantation (BMT) specialists. This is a retrospective review of the medical records of all HSCT recipients who were admitted to the MICU between January 1998 and June 2001. For those patients who were admitted more than once to the MICU during the same hospitalization, only the first MICU admission was analyzed.

Demographic, physiologic, and clinical data, including age, gender, race, underlying disease, type of HSCT (ie, allogeneic vs autologous), source of the stem cells (ie, related or unrelated), and human leukocyte antigen compatibility (ie, matched vs unmatched), were collected on admission to the MICU. Attempts were made to determine the indication for admission to the MICU based on clinical and laboratory parameters. In addition, laboratory data obtained within 24 h of admission to the MICU were collected. If the laboratory value was not available within 24 h of MICU admission, the most recent value obtained up to 72 h prior to MICU admission was used. These laboratory data included the following: WBC count; hematocrit; platelet count; BUN level; creatinine level; electrolyte levels; total bilirubin level; arterial blood gas measurements; serum lactate level; albumin level; and blood cultures. Chest radiograph findings also were recorded. The number of weeks since transplantation, and the number of days that the patient was in the hospital before admission to MICU also were included in the analysis.

APACHE (acute physiology and chronic health evaluation) II score and simplified acute physiology score (SAPS) II were recorded for each patient within the first 24 h after their admission to the MICU.2425 Based on the information available in the medical records, the authors made every attempt to determine the number and type of organ system failure during each patient’s MICU stay.

Organ-system failure was recorded if the patient had one or more of the following conditions occur during their MICU stay: respiratory failure (ie, the presence of hypoxemia or hypercapnia, or the need for intubation and MV); cardiovascular failure (ie, the occurrence of ventricular tachycardia or fibrillation, or the need for IV infusion of dobutamine, norepinephrine, vasopressin, or epinephrine at any dose, or for dopamine at > 5 µg/kg/min for at least 4 h); renal failure (ie, serum creatinine level, ≥ 3.4 mg/dL); neurologic failure (ie, Glasgow coma score of ≤ 6 when available, or subjective criteria such as the presence of confusion, decreased responsiveness, or coma in absence of sedation); and hepatic failure (total bilirubin level, ≥ 4 mg/dL). Absolute neutropenia was defined as a neutrophil count of < 500 cells/µL.

MICU data including MV (defined as endotracheal intubation and positive-pressure ventilation lasting for > 24 h), time of intubation in relation to admission to the MICU, and indications for MV also were reviewed. Data were also collected on procedures performed in the MICU, including bronchoscopy, open lung biopsy, pulmonary arterial catheterization, and hemodialysis. If the patient died, the mode of death, such as withdrawal of life support or failure to recover spontaneous circulation after adult cardiac life support (ACLS) protocol, was documented.

All patients were evaluated longitudinally to determine their MICU and hospital outcomes. In addition, the 6-month survival rate was recorded when data were available. Values were reported as the median and/or the mean ± SD. All percentages were approximated to round numbers. Parametric interval data were initially analyzed using a two-tailed Student t test. These data are listed as the mean ± SD. Nominal data were analyzed by {chi}2 analysis with Yates continuity correction or by Fisher exact test when appropriate.

Multiple logistic regression analysis was used to identify the variables that were independently associated with death. Each variable that was found to be significant at p < 0.05 by univariate analysis was introduced into a backward, stepwise, logistic regression model. A p value of < 0.05 was used to indicate statistical significance.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
During the study period, there were 745 patients who underwent HSCT, and 85 patients (11.4%) were admitted to the MICU. The baseline clinical characteristics of patients prior to admission to the MICU are summarized in Table 1 . The main indications for HSCT were hematologic disorder in 52 patients (61%) [non-Hodgkin lymphoma, 14 patients; acute myelogenous leukemia, 11 patients; chronic myelogenous leukemia, 10 patients; acute lymphoblastic leukemia, 5 patients; myelodysplastic syndrome, 6 patients; Hodgkin disease, 3 patients; aplastic anemia, 2 patients; and multiple myeloma, 1 patient]. Solid malignancy was the underlying disease category in 31 patients (36%) [advanced breast cancer, 26 patients; lung cancer, 2 patients; ovarian cancer, 1 patient; renal cancer, 1 patient; and brain cancer, 1 patient]. Two patients (3%) had systemic sclerosis and underwent autologous HSCT for the treatment of this condition. The median time from HSCT to admission to the MICU was 5 weeks. Fifty-five patients (65%) were admitted to the MICU within the first 100 days after undergoing transplantation, and 12 patients (14%) were admitted 1 year after undergoing transplantation. The median length of stay (LOS) in the hospital prior to MICU admission was 8 days (range, 0 to 64 days). There were no significant differences in any of the baseline clinical characteristics between survivors and nonsurvivors during MICU admission (Table 1).


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  		Table 1. Baseline Clinical Characteristics of all HSCT Recipients, Survivors, and Nonsurvivors Admitted to the MICU*

 
The median LOS in the MICU was 4 days (range, 1 to 75 days), and this was comparable between survivors (median LOS, 4 days) and nonsurvivors (median LOS, 5 days). Fifty-two patients (61%) were discharged alive from the MICU, and 35 patients (41% of all patients) were discharged alive from the hospital. The 6-month survival data were available on 76 patients (information was not available on 9 patients), of whom 21 (28%) were alive. Twelve patients (14%) had been readmitted to the MICU during the same hospitalization. Only one of those patients who had been readmitted to the MICU was discharged alive from the hospital.

Sixty-seven percent of those patients who died in the MICU (22 of 33 patients) died after the withdrawal of intensive support. Thirty-three percent of patients (11 of 33 patients) underwent the ACLS protocol. Only two of those patients survived the initial ACLS, however, they died later during the MICU stay.

The main indications for admission to the MICU are summarized in Table 2 . Pneumonia was the most common respiratory indication for MICU admission (18 patients). Other conditions included pulmonary edema, airway problems due to severe mucositis, diffuse alveolar hemorrhage, and pulmonary embolism. The main cardiac indications were arrhythmia (seven patients), pericardial effusion, myocardial infarction, and cardiac arrest prior to MICU admission. Seizure activity was the most common neurologic indication (three patients), while the other two patients had intracranial bleeding.


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  		Table 2. Main Indications by Organ System for MICU Admission for All HSCT Recipients, Survivors, and Nonsurvivors*

 
A total of 51 patients (60%) required intubation and MV during their stay in the MICU. Table 3 describes the clinical features of the patients who received mechanically ventilation. The median MICU LOS for mechanical ventilated patients was 7 days, compared to 3 days for those who did not require MV (p < 0.01). Nineteen of those mechanically ventilated patients (37%) survived their MICU stay, and only 10 (20%) were discharged alive from the hospital. This was in sharp contrast to patients who did not require MV (34 patients), of whom 33 patients (97%) were discharged from the MICU (p < 0.0001) and 25 patients (73%) were discharged alive from the hospital (p < 0.01). There were no significant differences in the indications or duration of MV between survivors and nonsurvivors.


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  		Table 3. Clinical Characteristics of HSCT Recipients Requiring Mechanical Ventilation*

 
Acuity scores and main laboratory variables on admission to the MICU were recorded and compared between survivors and nonsurvivors, as shown in Table 4 . The initial APACHE II score and SAPS II demonstrated significant differences between survivors and nonsurvivors (mean APACHE II score:survivors, 21 ± 6.7; nonsurvivors, 26.7 ± 7.4 [p < 0.01]; mean SAPS II: survivors, 14.8 ± 6.6; nonsurvivors, 20.4 ± 7.6 [p < 0.01]). Other MICU admission laboratory data that were significantly different between the two groups were platelet count, abnormal prothrombin time, partial thromboplastin time, serum lactate level, and positive blood culture results. The serum lactate level on admission to the MICU was significantly higher in patients who eventually died in the MICU (survivors, 1.9 ± 1.4 nonsurvivors, 4.0 ± 3.1 mmol/L; p < 0.01). Only five patients with serum lactate levels of > 3 mmol/L survived their MICU stay, and no patient admitted to the MICU with a serum lactate level of > 6 mmol/L survived.


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  		Table 4. Acuity Scores and Main Laboratory Variables on MICU Admission for Survivors and Nonsurvivors*

 
Twenty-nine patients (34%) had positive blood culture results either during the 24 h immediately prior to MICU admission, or within the first 48 h after MICU admission. Seven patients had more than one organism isolated from a blood culture. The most common isolates were Gram-positive cocci (22 patients), Gram-negative bacilli (9 patients), fungal isolates (3 patients), and viral isolates (3 patients). Patients with positive blood culture results had higher a mortality rate when compared to those with negative blood culture results (79% vs 24%, respectively; p < 0.001). No differences in outcome were observed based on the type of organism isolated.

Fifty-five patients (65%) had one or more organ systems fail, according to the criteria described in the "Materials and Methods" section. Mortality increased with the number of organ systems that failed (Table 5 ), and this trend was seen with all types of organ system failures (Fig 1 ). There was no absolute number of organ system failures that was associated with zero survival.


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  		Table 5. Number of Organ System Failures in Survivors and Nonsurvivors Who Were Admitted to MICU*

 


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  		Figure 1. Difference in the incidence of organ system failure between survivors (white segments) and nonsurvivors (black segments). * = p < 0.01.

 
The diagnostic and therapeutic interventions performed on patients during their MICU stay were reviewed. Twenty-four patients (28%) underwent bronchoscopy with BAL, and the procedure revealed a diagnosis in 13 patients (54%). Open lung biopsy was performed in five patients (6%). A diagnosis of diffuse alveolar damage was given in two patients, cytomegalovirus pneumonia was given in one patient, herpes simplex virus pneumonia was given in one patient, and bronchiolitis obliterans organizing pneumonia was given in one patient. Four of the patients who underwent open lung biopsy survived their MICU stay, and one died. Ten patients (12%) underwent pulmonary arterial catheterization to guide hemodynamic management. Three of those patients survived the MICU stay, while seven died (p = 0.04). Furthermore, 11 patients (13%) started treatment with hemodialysis in the MICU for the management of acute renal failure, and 3 of them survived and 8 died (p = 0.02).

To determine the predictors of MICU outcome, statistically significant physiologic and laboratory variables on MICU admission (Table 4), as well as the need for MV and the presence of multiorgan system failure (MOSF), were entered into a stepwise backward elimination regression analysis model. High serum lactate level on MICU admission, the need for MV, and the presence of more than two MOSFs during their MICU stay predicted poor MICU outcome (Table 6 ).


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  		Table 6. Predictors of MICU Mortality on Stepwise Backward Elimination Regression Analysis

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The aim of this study was to assess the outcomes of HSCT recipients who had been admitted to our MICU, and to identify the predictors of MICU adverse outcome for this group. The data showed that the MICU survival rate was 61%, while 41% of patients survived to hospital discharge and 28% were alive 6 months later. For those patients who required MV (60% of the patients), 37% survived their MICU stay and 20% were discharged alive from the hospital. Independent predictors of adverse MICU outcome in this patient population were MV, MICU admission serum lactate level, and the presence of MOSF.

During the study period, only 11.4% of patients who underwent HSCT required further management in the MICU, and only 7% received MV. These values are lower than those reported in earlier studies (24 to 40%)456717 for patients who required MICU admission, and around 25%8 required MV. This lower percentage is unlikely to be due to the underutilization of MICU resources, since in our institution all HSCT patients whose clinical status deteriorates are routinely transferred to the MICU for further monitoring and treatment. Rather, the observed decrease in MICU utilization is probably related to a shorter neutropenic phase, better antimicrobial prophylaxis and treatment, and improved experience in the management of these patients before their condition deteriorates. The fact that a significant number of our patients underwent autologous HSCT for the treatment of breast cancer, which is associated with a less intense conditioning regimen, may also have contributed to the lower percentage of patients requiring admission to the MICU. Nevertheless, these patients were critically ill on admission to the MICU, as illustrated by their high APACHE score and SAPS.

The clinical experience with BMT recipients requiring MICU admission has evolved over the last 2 decades (Table 7 ). Initial studies reported survival rates that approached 0%, especially for those who required MV, and as a result there were attempts not to offer these patients MV or even admission to the MICU.13 However, trends in MICU survival have shown steady improvement over the last several years, and our study further supports this trend. The reason for this improvement is probably multifactorial, and likely is related to improved prophylaxis and treatment of a variety of infections such as Pneumocystis carinii pneumonia, cytomegalovirus, and aspergillosis. Additionally, improved MV strategies that minimize further lung injury and MOSF have perhaps contributed to the improvement in the outcome of those who required MV.26 Furthermore, the routine use of peripheral blood instead of BMT probably has led to better engraftment and less need for immunosuppressive therapy.2728


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  		Table 7. Survival of Adult BMT Recipients Admitted to MICU and Literature Review*

 
Several studies have tried to identify the clinical variables at MICU admission that are associated with poor outcome (Table 7). Few studies have suggested that pre-MICU admission clinical characteristics (eg, age, type of transplant, presence of neutropenia or GVHD, or time from transplant to MICU admission) were important predictors of poor outcome, however, most of the studies, including our own, have shown that these pre-MICU admission characteristics are unreliable predictors of MICU outcome for this patient population. In addition, our study showed that measures of severity of illness such as APACHE II score and SAPS II have failed to predict outcome, which is an observation that has been made by others.1529

The outcome predictors that were consistently seen in most of the studies, and were confirmed by ours, are the need for MV, and the presence of MOSF. In our study, the need for MV increased the odds of death by 55.6 times, while the presence of more than two organ system failures increased the risk by 13.5 times, irrespective of the type of organ system failure. Furthermore, our investigation provided an additional prognosticator that has not been previously reported in this patient population, which is that an elevated serum lactate level on admission to the MICU was an independent predictor of poor MICU outcome. To our knowledge, our study is the first one to document this finding, which is a reflection of critical illness and may be an additional predictive tool for clinicians managing these patients.

The survival rate of HSCT recipients who have been admitted to the MICU is remarkably similar to that of other critically ill patient populations, such as those with sepsis-related ARDS.26 Furthermore, our study has shown that survival is related to serum lactate level and the number of organ system failures rather than the type of HSCT or the complications related to the transplant itself. This suggests that the outcomes of HSCT recipients who have been admitted to the MICU may be more dependent on their underlying critical illness than on the fact that they are transplant recipients. Consequently, it seems reasonable to manage these patients aggressively, in a manner that is similar to the treatment of other groups of patients with different critical illnesses. Nonetheless, it should be kept in mind that HSCT recipients are more prone to unique infectious and noninfectious complications, and that their organ systems tend to deteriorate rapidly.30313233

The survival rate was significantly lower among patients who required hemodialysis during their MICU stay (survival rate, 27%). This finding is, however, better than that reported by Scott et al22 and Jacobe et al,34 who indicated that the mortality rate was 100% in patients requiring hemodialysis in the MICU. In addition, the patients who required the insertion of a pulmonary artery catheter for hemodynamic and fluid management had a worse outcome (survival rate, 30%). These observations could simply reflect the fact that these patients were more acutely ill, with evidence of severe organ dysfunction warranting such interventions, thus yielding the increase in mortality rate.

Our study showed that none of the patients who underwent the ACLS protocol were discharged alive from the MICU. Although the number is small, this observation suggests that, while aggressive therapy is appropriate for this patient population, subjecting them to the ACLS protocol appears to be futile, and such an intervention probably should be avoided.

In conclusion, our data have shown that intensive care and MV for HSCT recipients should not be regarded as futile therapy. The short-term and long-term survival rates are steadily improving. There are no absolute predictors of MICU outcome, however, those patients with elevated serum lactate levels on admission to the MICU, those who require MV, or those who experience more than two organ system failures are less likely to survive.


   Acknowledgements
 
The authors thank Ms. Roze Kadri for her assistance in preparing the manuscript.


   Footnotes
 
Abbreviations: ACLS = adult cardiac life support; APACHE = acute physiology and chronic health evaluation; BMT = bone marrow transplantation; GVHD = graft-vs-host disease; HSCT = hematopoietic stem cell transplantation; LOS = length of stay; MICU = medical ICU; MOSF = multiorgan system failure; MV = mechanical ventilation; SAPS = simplified acute physiology score

Received for publication January 30, 2004. Accepted for publication May 5, 2004.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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