Abstract
Background:
Older adults with AML are often assumed to have poor outcomes following admission to the ICU. However, little is known about ICU utilization and post-ICU outcomes in this population.
Methods:
We conducted a retrospective analysis of 330 patients ≥ 60 years diagnosed with AML between 2005 and 2013 at two hospitals in Boston. We used descriptive statistics to examine the proportion of patients admitted to an ICU admission, as well as their mortality and functional recovery. We used logistic regression to identify risk factors for in-hospital mortality.
Results:
Ninety-six patients (29%) were admitted to the ICU, primarily due to respiratory failure (40%), septic shock (29%), and neurological compromise (9%). The proportion of patients that survived to hospital discharge, 90-days, and one-year were 47% (45/96), 35% (34/96), and 30% (29/96), respectively. At 90 days, 76% of patients had an Eastern Cooperative Oncology Group performance status (ECOG-PS) of 0 or 1 and 79% continued to receive AML-directed therapy. In multivariate analysis, poorer baseline ECOG-PS (OR 2.52, P=0.026) and need for two or more life-sustaining therapies (i.e. vasopressors, invasive ventilation and/or renal replacement therapy) were associated with increased odds of in-hospital mortality (OR 14.3, P<0.001).
Conclusions:
While almost one-third of older patients with AML were admitted to an ICU, nearly half survived to hospital discharge with good functional outcomes. Baseline performance status and the need for two or more life-sustaining therapies predict hospital mortality. These data support the judicious use of ICU resources for older patients with AML.
MeSH Keywords: acute myeloid leukemia, critical care, in-hospital mortality, activities of daily living
Precis for Table of Contents:
Older adults with AML experience high rates of ICU admission and nearly half of those admitted to the ICU survive to hospital discharge with good functional outcomes. Poor performance status and need for multiple life-sustaining therapies are important predictors of ICU mortality.
Introduction
Older patients with acute myeloid leukemia (AML) (aged ≥60 years) face a difficult disease with a poor prognosis a median survival of 8–10 months and low chance of long-term disease-free survival.1–3 Yet, a subgroup of older patients with AML can achieve long-term disease control, often by pursuing intensive therapies that carry a substantial risk of morbidity and mortality.1,2,4 These treatments can lead to life-threatening complications including the need to receive care in the intensive care unit (ICU). However, data on outcomes of older patients with AML requiring an ICU admission are lacking.
Prior studies have shown that patients with hematologic malignancies who are admitted to the ICU can have 90-day survival rates of approximately 50–60% with good functional outcomes.5–10 Two prior retrospective studies examined outcomes of younger AML patients (median age <55) receiving intensive chemotherapy who were admitted to the ICU. These studies have shown generally similar rates of survival.6,7 However, data are lacking on the outcomes of older (>60 years) patients with AML admitted to the ICU. Importantly, the impact of an ICU admission on the functional outcomes of older patients with AML is currently unknown. Given the known associations of older age and frailty with higher ICU morbidity and mortality, it is particularly important to define the potential role of critical care for older patients with AML.11–16
Over the past two decades, the frequency of ICU admissions for patients with hematologic malignancies have increased.5,8,17,18 As these trends continue and larger numbers of patients are considered reasonable candidates for critical care, it is essential to identify which patients are most likely to benefit from intensive care interventions. However, factors that are associated with ICU mortality for older patients with AML are currently unknown. An understanding of these factors has important clinical implications on clinicians’, patients’, and families’ decisions regarding intensive care utilization.
The objective of our study was to describe ICU utilization and outcomes for older patients (≥60 years) with AML. We also aimed to describe the functional outcomes for patients who survive to hospital discharge following an episode of critical illness. Finally, we sought to identify potential predictors of ICU mortality to better inform medical decision-making.
Methods
Study Design
We conducted a retrospective analysis of all patients aged ≥ 60 years who had a new diagnosis of AML and received treatment at the Dana-Farber Cancer Institute/Brigham and Women’s Hospital or Massachusetts General Hospital between May 1, 2005 and December 31, 2013. All patients received an initial diagnosis of AML within the years specified and had a minimum of 2-year follow-up from the time of their diagnosis. Patients receiving intensive induction therapy or non-intensive therapy at the time of diagnosis were included in the analyses. We defined intensive induction as receiving standard ‘7+3’ with a combination of cytarabine and an anthracycline or a modification of this regimen on a clinical trial with other agents added to the 7+3 backbone. We defined non-intensive therapy as receiving hypomethylating agents, low-dose cytarabine, or single agent therapy on a clinical trial. As one of our goals was to assess ICU outcomes among older patients with AML receiving active therapy, we excluded patients treated with supportive care alone. Patients admitted to the ICU at the time of diagnosis were included if they subsequently initiated treatment during the same hospitalization. As the majority of our patients (89%, 85/96) experienced only one ICU admission, we limited our analysis to the first ICU admission. We obtained 2-year follow-up data on all study participants to assess their ICU utilization after their initial diagnosis.
Data collection
We identified the eligible cohort using the Dana-Farber Cancer Institute and Massachusetts General Hospital’s Leukemia Clinical Research Information Systems database, which includes all patients with acute leukemia receiving treatment at these institutions. We categorized patients according to whether they were ever admitted to an ICU (medical, surgical, cardiac, or neurological/neurosurgical ICU). We then conducted a comprehensive chart review to obtain: demographics, comorbidities, AML disease risk, disease status at the time of ICU admission, and life-sustaining interventions employed (invasive ventilation, vasopressors and/or acute renal replacement therapy) during the ICU stay. We used the Hematopoietic Cell Transplantation-specific Comorbidity Index (HCT-CI) to assess comorbidities and the European Leukemia Net risk stratification to assess AML disease risk.4,19 HCT-CI was assessed by chart review as a baseline characteristic at the time of diagnosis. We also collected data on post-ICU care including the receipt of AML-directed therapy and mortality.
We collected data on patients’ performance status and functional status both pre- and post-ICU admission. To assess performance status, we used the Eastern Cooperative Oncology Group Performance Status (ECOG-PS). We defined functional status as either “dependent” or “independent” for all basic activities of daily living (ADLs). These included bathing, dressing, toileting, grooming, feeding and transferring. We used clinicians’ notes to capture information on both performance and functional status pre-ICU admission (within 90 days prior to ICU) admission, and post-ICU admission (90 to 180 days). ECOG-PS was usually documented explicitly. Functional status often had to be inferred from the narrative portion of clinicians’ notes, including those of oncologists, other physicians, physical therapists, social workers and visiting nurses. As ADLs were not recorded comprehensively in the medical record, dependence for any single ADL was considered “dependent.” Two coders independently reviewed all records to capture this information and obtained excellent inter-rater reliability (kappa = 0.90). We obtained patients’ pre-ICU ECOG-PS and functional status from electronic health record documentation within three months prior to ICU admission to reflect recent outpatient status.
Reason for ICU admission was determined by the disease process that initially prompted ICU transfer as documented in the ICU admission note. As in prior studies, we defined life-sustaining ICU therapies as vasopressors, invasive ventilation and/or acute renal replacement therapy (RRT) documented in the medical record at any time during ICU admission.5–8 Consistent with prior studies, only acute RRT, usually with continuous veno-venous hemofiltration (CVVH), was considered a life-sustaining ICU therapy. In-hospital mortality was defined as any death prior to discharge, including deaths in the ICU, step-down unit or regular hospital floor. One patient was discharge to home hospice. However, this patient lived for nearly a year and was not counted as an in-hospital mortality.
Statistical Methods
We used descriptive statistics to summarize patient and disease characteristics of all study patients stratified by ICU admission status. We also used descriptive statistics including frequencies and percentage to characterize the proportion of patients surviving after their ICU admission and functional recovery. We then conducted univariate analyses examining the association between a priori pre-defined demographic and clinical characteristics and in-hospital mortality after an ICU admission. These a priori characteristics were based on prior studies with the exception of ECOG-PS, which was selected on the basis of investigator consensus. We examined the following variables in the univariate analyses: age, sex, race, marital status, HCT-CI, pre-ICU functional and performance status, disease risk, initial treatment strategy (intensive induction versus non-intensive therapy), disease status at the time of ICU admission, time from diagnosis to ICU admission, and time from hospital admission to ICU utilization. Factors that were associated with p-value<0.10 in the univariate analyses were included in a multivariable logistic regression model to identify factors associated with in-hospital mortality. Age was a priori-defined as an important variable to include in the multivariable analyses. Due to co-linearity of ADL-dependence and ECOG-PS, we chose to keep ECOG-PS in the final model. We conducted all analyses in Stata 9.3 and considered a two-sided p-value < 0.05 to be statistically significant.
Results
Patient Characteristics
Table 1 depicts the clinical and demographic characteristics of all patients (n=330) included in this study. The median age of the cohort was 69 years (range 60–90) and their mean HCT-CI was 1 (range 0–9). Overall, 29.1% of patients (n = 96) were admitted to the ICU (Figure 1). The median age of patients admitted to the ICU was 67 (range 60–88) and their median HCT-CI score was 2 (range 0–7). There were no statistically significant differences in age, sex, race or ethnicity between patients admitted to the ICU and those not admitted the ICU. Of those admitted to the ICU, 55.2% (52/96) were receiving initial treatment for AML, 8.3% (8/96) were receiving consolidation therapy, 16.7% (16/96) were in CR and not receiving any therapy, and 19.8% (19/96) were receiving second or third line therapy for relapsed or refractory disease. Overall, 34.4% (33/96) of patients were admitted within 30 days of diagnosis, 30.2% (29/96) were admitted within 30–180 days of diagnosis, and 27.1% (26/96) were admitted >180 days after diagnosis.
TABLE 1:
Patient Characteristics
| All Patients (n = 330) |
Admitted to ICU (n= 96) |
No ICU Admission (n = 234) |
|
|---|---|---|---|
| Age, median (range) | 69 (60–90) | 67 (60–88) | 69.5 (60–90) |
| Male, n (%) | 195 (59.1%) | 55 (57.29%) | 140 (59.8%) |
| Hispanic ethnicity, n (%) | 11 (3.3%) | 2 (2.1%) | 9 (3.9%) |
| Religion, n (%) | |||
| Catholic | 144 (43.8%) | 37 (38.9%) | 107 (45.7%) |
| Other Christian | 100 (30.3%) | 30 (31.3%) | 70 (29.9%) |
| Muslim | 1 (0.30%) | 0 (0.0) | 1 (0.4%) |
| Jewish | 25 (7.6%) | 10 (10.5%) | 15 (6.4%) |
| None | 59 (17.9%) | 18 (18.9%) | 41 (17.5%) |
| Missing | 1 (0.30%) | 1 (1.0%) | 0 (0.0) |
| Race, n (%) | |||
| White | 321 (97.3%) | 93 (96.9%) | 228 (97.4%) |
| Asian | 3 (0.9%) | 1 (1.0%) | 2 (0.8%) |
| Black | 6 (1.8%) | 2 (2.1%) | 4 (1.7%) |
| Relationship status, n (%) | 36 (10.9%) | 10 (10.42%) | |
| Single | 243 (73.6%) | 74 (77.08%) | 26 (11.1%) |
| Married | 26 (7.9%) | 11 (11.46%) | 169 (72.2%) |
| Divorced | 25 (7.6%) | 1 (1.04%) | 15 (6.4%) |
| Widowed | 24 (10.3%) | ||
| Education, n (%) | 136 (41.2%) | ||
| High school or less | 150 (45.5%) | 39 (40.63%) | 97 (41.5%) |
| College | 44 (13.3%) | 43 (44.79%) | 107 (45.7%) |
| Post-grad | 14 (14.58%) | 30 (12.8%) | |
| HCT-CI, median (range) | 1 (0–9) | 2 (0–7) | 1 (0–9) |
| ELN Risk at Diagnosis, n (%) | |||
| Favorable | 25 (7.6%) | 6 (6.3%) | 19 (8.1%) |
| Intermediate | 165 (50.0%) | 50 (52.1%) | 115 (49.1%) |
| Adverse | 140 (42.4%) | 40 (41.6%) | 100 (42.8%) |
| Initial Therapy for AML, n (%) | |||
| Intensive | 197 (59.7%) | 72 (75.0%) | 125 (52.4%) |
| Non-intensive | 133 (40.3%) | 24 (25.0%) | 109 (46.6%) |
Figure 1:
Study Flow Diagram
ICU Admissions
The primary indications for ICU admission were respiratory failure (37/96, 40%), septic shock (27/96, 29%), neurological compromise (9/96, 9%), cardiogenic shock/myocardial infarction/arrhythmia (7/96, 7%), hemorrhagic shock (7/96, 7%) and other (9/96, 9%) (Figure 2). The “other” category included anaphylactic reaction, transfusion reaction, pulmonary embolism, DIC and two cases of febrile neutropenia that were determined to require particularly close monitoring (not generally an indication for ICU admission in the study institutions). Need for ICU transfer was determined by the treating physicians and the accepting ICU team. Of those admitted to the ICU, 49% (47/96) required invasive ventilation, 47% (45/96) required vasopressors, and 11% (11/96) required renal replacement. Overall, 26% (25/96) of patients experienced an ICU admission during the hospitalization when they were first diagnosed with AML, 24% (23/96) were in complete remission (CR) at the time of ICU admission and the remainder had an established diagnosis but were not in CR. The median time from hospital admission to ICU admission was 4.5 days (range 0–49) and 32% of patients were admitted to the ICU with 24 hours of hospital admission (31/96).
Figure 2:
Primary Indication for ICU Admission
Patient Outcomes following an ICU Admission
Of the 96 patients admitted to the ICU, 47% (45/96) were alive at the time of hospital discharge, 35% (n=34/96) were alive at 90-days, and 30% (29/96) were alive at one year (Figure 1). Of those alive at discharge, the majority, 64% (29/45), were still alive at one year. Notably, 62% (28/45) of patients who survived to hospital discharge either remained in CR or achieved CR after their ICU stay, and 24% (11/25) received further AML therapy without achieving a CR. Only 9% of patients (4/45) surviving to hospital discharge stopped receiving AML therapy despite having persistent leukemia.
Among patients alive 90-days post-ICU admission, 76% (26/34) had an ECOG-PS of 0 or 1 when assessed between 90 and 180 days post-ICU. Mean ECOG-PS post-ICU was 1.28 (± 0.22 SE) and the mean increase in ECOG-PS from baseline to 90 days post-ICU was 0.52 (± 0.21 SE, p=0.024). Of those alive at 90 days, 82% (28/34) were independent for all activities of daily living (ADLs) prior to their ICU stay, and 68% (23/34) remained independent at 90 days post-ICU hospitalization.
Factors associated with in-hospital mortality after an ICU admission
In unadjusted analyses (Table 2), the following factors were significantly associated with higher odds of in-hospital mortality: poorer pre-hospitalization ECOG PS, dependence on others for ADLs, need for vasopressors, need for invasive ventilation, and the need for two or more life-sustaining therapies. Of patients with pre-hospital ECOG PS < 2, 51.7% were alive at hospital discharge, compared with 21.4% of patients with pre-hospital ECOG PS ≥ 2. Of patient who required ≤ 1 life-sustaining therapy, 61.5% were alive at discharge, compared with 22.9% of patients who required ≥ 2 life-sustaining therapies. The proportion of patients alive at discharge whose primary ICU diagnosis was respiratory failure, septic shock, neurological compromise, hemorrhagic shock, or cardiogenic shock/MI/arrhythmia were 37.8% (12/37), 40.7% (11/27), 22.2% (2/9), 85.7% (6/7) and 57.1% (4/7) respectively.
TABLE 2:
Unadjusted Analyses of Factors Associated with In-Hospital Mortality
| Variable |
OR | 95% CI | P-value |
|---|---|---|---|
| Age | 1.02 | 0.95 – 1.08 | 0.618 |
| HCT-CI | 0.85 | 0.68–1.07 | 0.180 |
| White race | 1.11 | 0.74 – 1.67 | 0.609 |
| Relationship status – married | 0.93 | 0.36 – 2.41 | 0.879 |
| Life-sustaining therapies: | |||
| Vasopressors | 3.60 | 1.48–8.73 | 0.005 |
| Renal replacement therapy | 1.57 | 0.43–5.83 | 0.496 |
| Invasive Ventilation | 3.56 | 1.46–8.63 | 0.005 |
| Number of Life-sustaining therapies | |||
| Zero | Ref | ||
| One | 1.46 | 0.47 – 4.56 | 0.514 |
| Two or more | 8.19 | 2.51 – 26.73 | <0.001 |
| Baseline dependence for ADLs | 4.61 | 1.40 – 15.15 | 0.012 |
| Baseline performance status | 3.13 | 1.52 – 6.44 | 0.002 |
| Disease risk | 1.60 | 0.81 – 3.18 | 0.179 |
| Non-intensive therapy | 1.32 | 0.52 – 3.36 | 0.555 |
| Complete remission at ICU admission | 0.95 | 0.37 – 2.43 | 0.917 |
| ICU admission during initial diagnosis hospitalization |
0.31 |
0.12 – 0.80 |
0.016 |
| ICU care < 24 hours after hospital admission | 0.62 | 0.26–1.57 | 0.282 |
Patients admitted to the ICU during the hospitalization when they were initially diagnosed with AML had lower odds of in-hospital mortality compared to those who already had an established diagnosis. The proportion of patients alive at hospital discharge based on their treatment status was as follows: 54.7% for those receiving initial treatment, 50.0% for those receiving consolidation therapy, 43.8% for those in CR without active treatment, and 26.3% for those with relapsed disease.
In our multivariate analysis (Table 3), the following factors were independently associated with increased odds of in-hospital mortality: poorer ECOG PS prior to ICU admission (OR 2.76, 95% CI 1.24–6.12, p=0.013), and the need for two or more life-sustaining therapies (OR 12.39, 95% CI 3.10–49.48, p<0.001).
TABLE 3:
Multivariate Logistic Regression of Factors Associated with In-Hospital Mortality after ICU Admission
| Variable |
OR | 95% CI | P-value |
|---|---|---|---|
| Age | 1.04 | 0.95–1.14 | 0.423 |
| Number of life sustaining therapies | |||
| Zero | Ref | ||
| One | 2.57 | 0.66–10.06 | 0.174 |
| Two or more | 12.39 | 3.10–49.48 | <0.001 |
| Baseline performance status | 2.76 | 1.24–6.12 | 0.013 |
| ICU admission during initial diagnosis hospitalization |
0.47 |
0.12–1.87 |
0.287 |
Discussion
This study demonstrates that older adults with AML experience high rates of ICU admission, nearly twice that of younger patients with AML.6 Of those admitted to the ICU, nearly half survive to hospital discharge and a substantial minority survive up to one year after an ICU admission with good functional outcomes and disease control. We identify poor performance status prior to ICU admission and the need for two or more life-sustaining therapies as strong predictors of ICU mortality in this population. These data demonstrate the potential role for ICU care in older patients with AML and highlight the complexity of medical decision-making for managing their critical illness.
Despite their age and increased potential for frailty and comorbidities, our study demonstrates that older patients with AML have comparable rates of surviving to hospital discharge after an ICU stay when compared to all adults with hematologic malignancies. Prior literature suggests that approximately 50–60% of all adults with hematologic malignancies admitted to the ICU survive to hospital discharge, compared with 47% in our cohort.5,20,21 These findings underscore that age alone should not be used as a contraindication to ICU admission for older patients with AML and highlight the need for a more accurate assessment of prognosis after an episode of critical illness in this population.
We also demonstrated that older patients with AML surviving an ICU stay experienced minimal decline in their performance status. This is remarkable for any post-critical care population, especially older adults with cancer.11 Importantly, the majority of these patients remained independent in all of their ADLs and only a minority were not able to receive further AML therapy, further underscoring the importance of providing critical care for this population. While most patients ultimately died from the sequelae of marrow disease, approximately a third survived up to one year after their ICU hospitalization with encouraging functional outcomes. These data can better inform clinicians, patients, and families in discussing the outlook for those older patients facing an ICU admission.
In addition, patients’ baseline performance status and the number of life-sustaining therapies employed in the ICU emerged as important factors that can help clinicians better prognosticate when older AML patients are facing an ICU admission. Prior studies in patients with hematologic malignancies have shown that a crude assessment of performance (bedbound versus not) was also predictive of ICU mortality.5 Clinicians can easily assess and record performance status making this a practical adjunct for critical care decision-making. Additionally, in prior studies of patients with hematologic malignancies, the need for more than one life-sustaining therapy was associated with higher in-hospital mortality.5,7–10 Similarly, in our cohort of older patients with AML, the need for two or more life-sustaining therapies portended a particularly poor prognosis that should be incorporated in clinical discussions with patients and families.
These findings have important implications for clinicians caring for older patients with AML, as they may use these data to better inform their discussions regarding treatment risk, the potential need for ICU care during AML therapy, and the overall outlook after an ICU hospitalization. These data can justify providing ICU-level of care for older patients with AML as long as it is consistent with patients’ and families’ wishes, since a significant proportion of these patients will survive and have reasonable functional outcomes. On the other hand, for those requiring two or more life-sustaining treatments, frank family discussions regarding their poor prognosis may have utility and impact their end-of-life decision-making.
Our study has several important limitations. First, the population included mostly white, educated patients receiving their care at two tertiary care centers in Boston, thus limiting the generalizability of our findings. Second, criteria for ICU admission are not standardized at the study institutions and tertiary care centers generally have a higher threshold for ICU admission than community hospitals, further limiting generalizability. Moreover, the patients admitted to the ICU may reflect a population that was thought likely to benefit from intensive care, as opposed to those counseled to pursue comfort measures only. Nonetheless, our findings are likely applicable to the care of many older patients with AML receiving their care at various medical centers. Third, our findings are limited by the nature of the retrospective chart review used to assess certain outcomes such as performance and functional status. Nonetheless, we used two independent coders with excellent inter-rater reliability to enhance the rigor of capturing these elements from the electronic medical record. Fourth, we did not have an assessment to measure frailty or patient-reported quality of life, important metrics to consider for older patients with cancer. Frailty in particular has been shown to be an important predictors of outcomes in hematologic malignancies.14–16 While functional status is one component of frailty, additional measures such as weight loss or falls were not recorded reliably in our medical record. Fifth, limited data in our medical records also precluded retrospective calculation of ICU illness severity scores such as APACHE (Acute Physiology, Age, Chronic Health Evaluation) or SOFA (Sequential Organ Failure Assessment). Fifth, while our database includes most patients with AML receiving care at our institutions, it is possible that a few patients with AML were admitted directly to the ICU and were never registered in the database and thus were not included in this analysis. Finally, patients may have received care, including ICU admissions, outside of our institutions that was not fully captured by our medical records.
In conclusion, older adults with AML are frequently admitted to the ICU and nearly half survive to hospital discharge. Those who survive often experience good functional outcomes, continue to pursue treatment for AML, and obtain disease control. Importantly, patient’s performance status prior to ICU admission and the need for two or more life-sustaining therapies emerged as important prognostic factors that were associated with ICU mortality. These findings support the judicious use of ICU resources for older patients with AML, particularly those with good performance status, and can better inform patient-clinician discussions regarding ICU outcomes in this population.
Funding:
this work was supported by funds from the National Cancer Institute Federal Share Program (El-Jawahri), and K24 CA 181253 (Temel).
Footnotes
Conflicts of Interest: None
References:
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