Organ transplantation has changed the way we approach patients with end-stage organ failure. Patients who would have otherwise died can live long, high-quality, and productive lives after receiving an organ transplant. In 2007 alone, 28,345 patients received organ transplants in the United States. Transplantation is successful: among patients receiving transplants in 2006, 1-year survival exceeded 80% for patients receiving heart and liver transplants (1). Unfortunately, each day, an average of 18 patients also die while awaiting organ transplantation because of inadequate organ supply (2).
Organ transplantation is a prime example of high-intensity healthcare. The procedures are complex, risky, and costly, with an estimated mean cost per transplantation of more than $160,000 (3). Although the outcomes of transplantation have dramatically improved over the past two decades, and for some organs transplantation has become a nearly routine next step for patients with end-stage disease, many patients have a difficult posttransplantation course, sometimes resulting in death.
A difficult challenge in providing high-quality end-of-life care to patients considered for transplantation is the dilemma of some patients who experience an extended decline with risk of death while being considered for transplantation. Others have a prolonged course after transplantation. For instance, in a cohort of 521 patients, 13% of liver transplant recipients had a hospital length of stay of more than 30 days. Prolonged length of stay was associated with postoperative infection, allograft rejection, gastrointestinal bleeding, renal failure, and decreased survival as well as higher cost and resource use (4).
Despite extensive patient preparation for transplantation, one study suggests that advance care planning (ACP), which is discussing a patient’s clinical condition and prognosis and mapping out future care according to a patient’s preferences, is underutilized in the transplant population. A survey of 155 patients undergoing hematopoietic cell transplantation revealed that 63% had discussed wishes regarding life support with their family and friends, but only 16% had discussed these wishes with their physicians and only 39% had an advance directive in their medical record (5). Little is known about ACP or palliative care among patients who die while being considered for transplantation.
Multiple studies show that patients value pain and other symptom management, communication with their physician, and preparation for future care as they approach the end of life (6–11). These issues are particularly salient among patients with end-stage organ failure. Even if the goal is survival, as is always the case in patients considering transplantation, patients rarely desire to receive high-intensity care at all costs. One survey of adults found that they rated certain clinical outcomes (severe pain, severe stroke, dementia, and permanent coma) as worse than death (12). In another study, patients were less likely to desire aggressive care if their clinical outcome would be more impaired than their current health state (13). Patients desire less aggressive treatment if they have a worse prognosis (14, 15) or will end up cognitively impaired (16).
Therefore, it is critical that complex and seriously ill patients, including those awaiting and receiving transplants, engage in ACP and receive high-quality symptom management during the course of their treatment. This is consistent with an evolving palliative care literature that shows benefits for concurrent palliative and curative care for patients with life-limiting illness (17, 18). In this article, we compare ACP and supportive care provided to a decedent population for whom transplantation was considered during the hospitalization versus other decedents at one academic medical center by evaluating the Assessing Care of Vulnerable Elders quality indicators for end-of-life care (19) and other care and outcomes relevant to end-of-life care (e.g., whether a patient received a palliative care consult).
The 496 decedents had an average age of 62 years, 47% were female, 62% were white non-Hispanic, and 60% were married. Most patients had either private insurance (45%) or Medicare (41%), with only 9% having Medicaid and 5% uninsured/self-pay/other. More than half had an end-stage disease on admission, with advanced cancer (21%) and end-stage liver disease (16%) being most common. Twenty-five percent of the sample were considered for transplantation (including patients listed as a transplant candidate as well as under active consideration/evaluation as documented in the medical record) during the terminal hospitalization (14% liver with or without bowel, 3% liver and kidney, 3% heart, 3% bone marrow, and 2% lung). The detailed characteristics of this sample have been reported previously (19).
Consideration of Transplantation and Quality of End-of-Life Care
Overall, 496 patients were eligible for 3086 quality indicators (mean, 6.2 per patient) and overall end-of-life quality of care was 70% (range, 25–100%) (19). The 126 patients considered for transplantation were eligible for 796 quality indicators (mean, 6.3 per patient) and their overall end-of-life quality of care was 65%, which was 7% lower than the quality of end-of-life care received by patients not considered for transplantation. Although pain and dyspnea management pass rates were similar whether or not they were considered for transplantation, patients considered for transplantation received less recommended care within the goals of care domain. For example, whereas patients not considered for transplantation had a timely discussion of goals of care on admission to the intensive care unit (ICU) 53% of the time, this occurred for patients considered for transplantation only 31% of the time (Table 1).
In bivariate analyses, factors other than considered for transplantation that also were associated with lower end-of-life care quality included Hispanic ethnicity, not having religion documented in the medical record, being admitted to the liver service, and being admitted to a surgical ICU. Patients with advanced cancer and patients admitted to the oncology service received significantly higher-quality of end-of-life care.
In a linear regression model that included all patient characteristics, patients considered for transplantation during the admission received 7% lower-quality end-of-life care compared with patients not considered for transplantation (P=0.02). The lack of documentation of a patient’s religion in the medical record was associated with a 10% lower quality score compared with Christian/Protestant patients (P=0.02; Table 2). In a linear regression model that included clinical service, patients admitted to a surgical intensive care service received 9% lower quality compared with patients admitted to a medical service (P=0.03; Table 3).
Consideration of Transplantation and Clinical Care and Outcomes Among Patients Dying an “Expected Death”
Of 496 patients studied, 424 (85%) had medical record documentation of an expected death. Expected death documentation was similar in patients considered and not considered for transplantation (84.9% vs. 85.7%, respectively; P=0.88). The mean timing for this documentation was 9 days before death in both groups.
Considering only those who died an expected death, consideration of transplantation was associated with less use of comfort orders at the end of life (32% vs. 64%; P<0.0001), lower rates of palliative care consultation (2% vs. 7%; P=0.01), and lower rates of early goals of care discussion within 48 hr of admission (20% vs. 39%; P<0.0001). Patients considered for transplantation also had a longer hospital stay before death (31 vs. 21 days; P=0.01), were more likely to be admitted to the ICU (95% vs. 77%; P<0.0001), were more likely to receive mechanical ventilation (89% vs. 69%; P<0.0001), and were more than twice as likely to have hemodialysis initiated for the first time during their terminal hospitalization (65% vs. 24%; P<0.0001; Table 4). With the exception of palliative care consultation, all of these associations remained significant in multivariate logistic models controlling for patient gender, age, race, ethnicity, presence of noncancer end-stage disease, and presence of advanced cancer.
Some patients considered for transplantation who clinically worsen are removed from transplant consideration, whereas others continue to be considered for transplantation despite a waning chance of survival. We evaluated whether explicit documentation that a patient was removed from consideration of transplantation reduced the likelihood of receiving poor-quality end-of-life care. Nearly half of patients (62 of 126 [49%]) who were considered for transplantation during the hospitalization had medical record documentation removing them from transplant consideration before death. Patients were removed from transplant consideration a median of 7 days before death (range, 0–158 days). Quality of care was not significantly different between patients removed and those never removed from transplant consideration (P=0.5). Receipt of clinical care was similar between patients who died without documentation withdrawing them from transplant consideration and patients removed from consideration of transplantation, although patients who were never removed from consideration received higher rates of ICU use (100% vs. 90%; P=0.01), mechanical ventilation (95% vs. 82%; P=0.02), and new hemodialysis (72% vs. 53%; P=0.03) during the terminal hospitalization.
Patients with end-stage disease who are being considered for organ transplantation would be expected to desire and receive the most aggressive treatments while they are maintained alive awaiting a life-saving organ. However, this study suggests that even when their physicians expect them to die they receive less comfort-oriented care than other dying patients. Goals of care discussions were less common among patients considered for transplantation, perhaps related to providers assuming that aggressive care was desired. However, without goals of care discussions, active transition to comfort-oriented care is less likely to occur in a timely manner, as demonstrated among patients considered for transplantation. Yet, death could have been anticipated as a possible outcome at hospital admission for nearly all these patients. These findings suggest that mechanisms are needed to foster better care at the end of life for patients considered for transplantation.
This is the first study to evaluate the quality of end-of-life care provided to patients who died while awaiting transplant, and the data suggest that such patients have greater unmet needs for palliative care compared with other decedents. Although all decedents in this sample received relatively aggressive care during their terminal hospitalization, patients considered for transplantation were less likely to receive palliative care consults and comfort care orders near death.
Increasing evidence suggests that ACP and symptom management can successfully be provided concurrently with potentially life-extending care. Temel et al. (17) showed in a randomized controlled trial that patients with advanced non–small cell lung cancer treated concurrently with palliative care had no decrease in survival and experienced improved symptom control compared with usual care. The ENABLE II randomized controlled trial also showed that palliative care improved quality of life and mood without affecting survival (18). Concurrent palliative care for patients awaiting possible transplantation should be considered.
Other factors associated with less good end-of-life care were receiving care on a surgical service and lack of documentation of religion. The surgical service quality deficit is consistent with the relative lack of emphasis on supportive care in surgical practice. The religion documentation finding raises several considerations, including the fact that nurse chart abstractors reviewed all notes in the medical record including social work and chaplain notes. Therefore, the lack of documentation of religion may have been a marker for less interdisciplinary care.
Our study has several limitations, mainly that we evaluated only patients who died; patients with similar levels of sickness who survived were not evaluated, although attention to symptom control and preferences is important for this group of patients as well. Although abstracted reliably from medical records, the definition of expected death may not be the same for transplant candidates and those not considered for transplantation, which may affect comparisons of process of care between these groups. In addition, the high correlation between disease type and clinical service made it infeasible to include these factors in the same regression equations, making it difficult to disentangle whether patient or provider factors are more important in determining quality of end-of-life care. Furthermore, this is a study of a single institution, albeit a leading transplant center; an evaluation of other hospitals is needed.
These data suggest room for improvement in symptomatic control for and communication with patients who died in the setting of being considered for transplantation. Recent reconceptualization of supportive care to become concurrent with desired survival-oriented care could improve the dying experience for these very ill patients. Earlier consideration of all potential outcomes and concurrent focus on symptom palliation will help address the care needs of the dying patient who is or was recently considered for transplantation.
MATERIALS AND METHODS
Study Design and Hypothesis
We used a retrospective observational study design to test our hypothesis that patients considered for transplantation will receive lower-quality ACP and end-of-life care.
We identified all patients ages 18 years or older who died during admission to one medical center between April 2005 and April 2006 following a hospitalization of at least 3 days. Of 500 patients who died during the study period, complete records were available for 496. A decedent sample was selected because we were interested in understanding how care is provided during a terminal hospitalization. Because all patients died before study initiation, the investigation was exempted from institutional review board approval (G06-09-025-01).
Measuring Quality of Care
A subset of measures from the Assessing Care of Vulnerable Elders-3 set was adapted for application to patients who died in the hospital. Sixteen quality indicators focused on three domains of end-of-life care: eliciting goals of care, pain assessment and management, and dyspnea assessment and management. These were applied to a diverse adult inpatient decedent sample (19).
The data elements needed to implement these quality indicators were collected by an abstraction of a full set of inpatient medical records by experienced nurse abstractors (19). Ten percent of the medical records were randomly selected to be abstracted a second time by a different nurse. Reabstraction revealed that 92% of quality indicators were triggered identically (pooled κ=0.67) and scoring for identically triggered quality indicators had 90% agreement (pooled κ=0.67).
Patient Data, Clinical Care, and Outcomes
We also collected from medical records patient characteristics, including demographics (age, gender, race, ethnicity, primary insurance, and religion), social support variables (marital status and preadmission living arrangement), clinical variables (presence of end-stage disease, mental status on admission, and consideration of transplantation), and ACP variables (discussions about preferences concerning end-of-life care, decision-making, and advance directives). If it was documented in the medical record that a patient was listed as a transplant candidate or under active consideration or evaluation for transplantation, the patient was identified as being considered for transplantation. This variable was abstracted with 96% agreement (κ=0.89). Because we were unable to identify individual physicians responsible for a specific patient due to the team-based approach to inpatient care, we collected the patient’s primary clinical service during the hospitalization. We also collected from medical records whether a patient died an “expected death.” Expected death was defined as any physician documentation during the terminal hospitalization that the patient was terminal, had a grave prognosis, was receiving hospice care, had imminently life-threatening disease in the context of a poor prognosis, or was dying. The specific criteria were reliably abstracted from the medical record (reabstraction κ=0.67; 91% agreement).
We evaluated the percentage of patients who received the care process prescribed in each of the 16 quality indicators and compared between patients who were transplant candidates and those who were not. For each patient, we then calculated an overall patient-level quality score. Because patients triggered different quality indicators and quality indicators had varying pass rates, the observed quality score for each decedent was compared against the expected score of a hypothetical patient who had triggered the identical quality indicator pattern to compute an observed-minus-expected (O-E) score (20). This O-E score was normally distributed allowing for standard OLS regression. Bivariate relationships between quality of care and patient characteristics (age, sex, race, ethnicity, religion, insurance status, marital status, pre-hospital venue, mental status on admission, and presence of end-stage disease on admission) and clinical service were studied. Multivariate regression models studying O-E quality as the outcome were chosen a priori based on what was hypothesized to potentially impact quality, with the transplant variable being the primary regressor of interest. Because specific end-stage disease was highly correlated with clinical service (cancer and oncology service, liver disease, or transplant with liver service; all r’s>0.6 and P’s<0.001), we evaluated the association of quality with clinical service in a separate regression equation.
In addition to examining quality scores, we also compared the clinical care and outcomes of decedents who were considered for transplantation with those who were not after limiting both groups to those patients who died an expected death. First, we compared rates of expected death between patients who were considered for transplantation and those who were not during the terminal hospitalization. We then explored bivariate relationships between transplant status and clinical care and outcomes of interest. Next, we studied these relationships in multivariate logistic regression models controlling for age, gender, race, ethnicity, and disease status.
We also conducted sensitivity analyses to evaluate if never being removed from consideration of transplantation affected the quality of end-of-life care. Analyses were performed with SAS statistical software version 9.2 (SAS, Cary, NC).
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