This qualitative study describes the end-of-life care attitudes, beliefs, practices, and discussions reported by patients with decompensated cirrhosis and the clinical team at liver transplant centers.
Key Points
Question
How is advance care planning experienced by patients with decompensated cirrhosis and clinicians at liver transplant centers?
Findings
In this qualitative study of 46 transplant center clinicians and 42 patients with decompensated cirrhosis, semistructured interviews found that despite patient interest in discussing end-of-life issues, few such conversations occurred between patients and clinicians. Conversations focused on the need for liver transplant rather than on end-of-life decision-making, with which surrogate decision makers often struggled.
Meaning
Results of this study suggest that substantial deficits exist in advance care planning for patients with decompensated cirrhosis at transplant centers; these gaps may help explain the suboptimal end-of-life care in this population.
Abstract
Importance
The burden of end-of-life care for patients with cirrhosis is increasing in the US, and most of these patients, many of whom are not candidates for liver transplant, die in institutions receiving aggressive care. Advance care planning (ACP) has been associated with improved end-of-life outcomes for patients with other chronic illnesses, but it has not been well-characterized in patients with decompensated cirrhosis.
Objective
To describe the experience of ACP in patients with decompensated cirrhosis at liver transplant centers.
Design, Setting, and Participants
For this multicenter qualitative study, face-to-face semistructured interviews were conducted between July 1, 2017, and May 30, 2018, with clinicians and patients with decompensated cirrhosis at 3 high-volume transplant centers in California. Patient participants were adults and had a diagnosis of cirrhosis, at least 1 portal hypertension–related complication, and current or previous Model for End-Stage Liver Disease with sodium score of 15 or higher. Clinician participants were health care professionals who provided care during the illness trajectory.
Main Outcomes and Measures
Experiences with ACP reported by patients and clinicians. Participants were asked about the context, behaviors, thoughts, and decisions concerning elements of ACP, such as prognosis, health care preferences, values and goals, surrogate decision-making, and documentation.
Results
The study included 42 patients (mean [SD] age, 58.2 [11.2] years; 28 men [67%]) and 46 clinicians (13 hepatologists [28%], 11 transplant coordinators [24%], 9 hepatobiliary surgeons [20%], 6 social workers [13%], 5 hepatology nurse practitioners [11%], and 2 critical care physicians [4%]). Five themes that represent the experiences of ACP were identified: (1) most patient consideration of values, goals, and preferences occurred outside outpatient visits; (2) optimistic attitudes from transplant teams hindered the discussions about dying; (3) clinicians primarily discussed death as a strategy for encouraging behavioral change; (4) transplant teams avoided discussing nonaggressive treatment options with patients; and (5) surrogate decision makers were unprepared for end-of-life decision-making.
Conclusions and Relevance
This study found that, despite a guarded prognosis, patients with decompensated cirrhosis had inadequate ACP throughout the trajectory of illness until the end of life. This finding may explain excessively aggressive life-sustaining treatment that patients receive at the end of life.
Introduction
Cirrhosis is a leading cause of mortality in the US, and the annual number of deaths among individuals with cirrhosis increased by 65% from 1999 to 2016.1 Addressing the patterns of end-of-life care in this population has gained growing attention.2,3,4 In the US, although more than half of patients with life-limiting illness die at home or on hospice care,5 60% of patients with cirrhosis die in an inpatient facility, a nursing home, or a long-term care facility.6 People with decompensated cirrhosis frequently receive burdensome care; more than half of them are mechanically ventilated and 16% receive hemodialysis during terminal hospitalizations.2 Liver transplant is a successful treatment, and 148 centers performed 8896 liver transplants in 2019.7 However, a transplant is not an option for most patients because of organ shortages and because many patients are not suitable candidates.8
Despite having similar life expectancy as patients with other advanced illnesses, patients with decompensated cirrhosis express preferences that are aimed at more aggressive end-of-life care.9 Advance care planning (ACP) conversations support patients in sharing their values, goals, and preferences in the context of their prognosis and future health states and have been associated with improved end-of-life outcomes.10 These outcomes include better patient quality of life, less health care utilization, and less bereavement.11,12 The rate of documented ACP is low in this population, but little explanation exists for why this is the case and few descriptions are available regarding the context of the ACP conversations that do happen.13,14,15
The aim of this study was to describe the experience of ACP in patients with decompensated cirrhosis at liver transplant centers, which have the highest volume of patients with this disease and the greatest resources for managing these patients. To this end, we used qualitative analyses of patient and clinician reports.
Methods
In this qualitative study, we purposefully sampled patients with decompensated cirrhosis and clinicians from 3 transplant centers in California with differing organizational structures, affiliations, and patient populations (eTable in the Supplement). The institutional review board of each transplant center approved this study. Written informed consent was obtained from all participants, and each informant received an honorarium.
Included patients met the following eligibility criteria: (1) adults aged 18 years or older with ability to provide informed consent and complete an interview in English, (2) diagnosis of cirrhosis, (3) diagnosis with at least 1 portal hypertension–related complication (ascites, variceal hemorrhage, or hepatic encephalopathy), and (4) current or previous model for end-stage liver disease with sodium (MELD-Na) score of 15 or higher (score range: 6-35, with the lowest score indicating a 90-day mortality of <2% and the highest score indicating a 90-day mortality of 65%-66%16).17,18 Patients with hepatocellular carcinoma were excluded because previous studies showed that their receipt of palliative care was different from that of other patients with decompensated cirrhosis.2,19,20,21 Patients were excluded if they demonstrated signs of moderate to severe hepatic encephalopathy, defined as a West-Haven score of 3 or higher. We sampled patients from each of the following strata, based on status at the time of interview: (1) too early (not sick enough) for transplant evaluation; (2) currently undergoing evaluation for transplant; (3) wait-listed for transplant; and (4) not wait-listed for transplant because of contraindications such as age, comorbid conditions, psychosocial barriers, or substance use. Patients were identified through electronic health record review, and eligibility was confirmed with the clinician during a clinic visit.
Clinicians were defined as health care professionals who were responsible for providing care during any component of a patient’s illness trajectory. We sampled the following clinicians: (1) transplant hepatologists, (2) transplant and hepatobiliary surgeons, (3) transplant coordinators, and (4) social workers.22,23,24
Interviews
Interview guides were developed to explore the context, behaviors, thoughts, and decisions of patients and clinicians regarding elements of ACP (prognosis, health care preferences, values and goals, surrogate decision-making, and documentation) as well as discussions at the end of life.25,26,27 Interview guides contained lead-in questions followed by probes, were pilot-tested with 10 informants (8 clinicians and 2 patients), and revised.
One of us (A.A.P.) conducted all 88 face-to-face semistructured interviews between July 1, 2017, and May 30, 2018. Clinicians were approached for participation either in person or by email. Interviews were audio-recorded, transcribed, and imported into NVIVO, version 12.0 (QSR International), for analysis.
Data Analysis
The primary goal of the analysis was to describe how ACP was implemented by clinicians and experienced by patients. Analyses proceeded in 2 stages. In the first stage, a team comprising a hepatologist (A.A.P.) and an experienced qualitative researcher in palliative care (D.T.) developed a code book using codes corresponding to major elements of ACP. Next, the team assigned codes to segments of text to identify all experiences pertaining to ACP in transcripts. Regular meetings were held to discuss and resolve all coding discrepancies and to combine codes. A pile-sorting technique was used to generate themes separately for patient and clinician transcripts.
In the second stage, identified themes were combined and compared to generate a final set that represented the range of ACP experiences. Thematic saturation occurred after 18 patient and 21 clinician interviews. Presentations with opportunities for feedback were given to all participating transplant teams as well as to transplant and nontransplant center clinicians from outside the 3 participating centers to ensure trustworthiness.
Results
Of the 63 patients contacted, 42 participated, of whom 11 (26%) were wait-listed for transplant, 9 (21%) were undergoing evaluation for transplant, 10 (24%) were too early for transplant, and 12 (29%) were not wait-listed for transplant because of comorbid conditions, active substance use, or psychosocial issues (Table 1). Eight patients did not have enough time for an interview, 7 did not show up for their scheduled interview, 3 were tired or not interested, and 3 gave no specific reason. The 42 patients had a mean (SD) age of 58.2 (11.2) years and consisted of 28 men (67%) and 14 women (33%) (Table 1). Patients had a mean (SD) MELD-Na score of 15.9 (7.3).
Table 1. Patient Characteristics .
| Characteristic | No. (%) |
|---|---|
| Age, mean (SD), y | 58.2 (11.2) |
| Sex | |
| Male | 28 (67) |
| Female | 14 (33) |
| Race/ethnicitya | |
| Hispanic or Latino | 17 (40) |
| Non-Hispanic | |
| White | 16 (38) |
| Black | 2 (5) |
| Asian | 1 (2) |
| Other or unknown | 6 (14) |
| Insurance status | |
| Medicare | 21 (50) |
| Private | 15 (36) |
| Medicaid | 6 (14) |
| Marital status | |
| Married or has life partner | 23 (55) |
| Single | 10 (24) |
| Divorced | 5 (12) |
| Widowed | 4 (10) |
| Cause of cirrhosisb | |
| Nonalcoholic steatohepatitis | 14 (33) |
| Alcohol related | 12 (29) |
| Hepatitis C | 11 (26) |
| Autoimmune hepatitis | 4 (10) |
| Other, cryptogenic, or unknown | 5 (12) |
| Manifestations of portal hypertension | |
| Ascites | 32 (76) |
| Hepatic encephalopathy | 29 (69) |
| Variceal hemorrhage | 8 (19) |
| MELD-Na score at time of interview, No. (SD)c | |
| 6-10 | 13 (31) |
| 11-14 | 5 (12) |
| 15-20 | 12 (29) |
| 21-30 | 10 (24) |
| 31-40 | 2 (5) |
| Child-Pugh scored | |
| 5-6 (A) | 5 (12) |
| 7-9 (B) | 22 (52) |
| 10-15 (C) | 15 (36) |
| Transplant status | |
| Wait-listed for transplant | 11 (26) |
| Undergoing evaluation for transplant | 9 (21) |
| Too early for transplant evaluation | 10 (24) |
| Not wait-listed for transplant | |
| Because of comorbidities | 6 (14) |
| Because of active substance use or psychosocial issues | 6 (14) |
Abbreviation: MELD-Na, model for end-stage liver disease with sodium.
As reported in the electronic health record.
Three patients had more than 1 cause for cirrhosis.
A higher MELD-Na score indicates a greater likelihood of dying in 3 months.
A higher Child-Pugh score indicates a greater likelihood of dying in 1 year.
Of the 66 clinicians contacted, 46 participated, of whom 13 (28%) were hepatologists, 11 (24%) were transplant coordinators, 9 (20%) were hepatobiliary surgeons, 6 (13%) were social workers, 5 (11%) were hepatology nurse practitioners, and 2 (4%) were critical care physicians. Three clinicians were not interested in being interviewed, 4 had scheduling conflicts, and 13 did not respond to the invitation.
Table 2 shows example questions from the interview guides. These questions were adjusted between interviews.
Table 2. Topic and Example Questions From Interview Guidesa.
| Broad topic | Specific topics | Example questions |
|---|---|---|
| Patient | ||
| Lead-in questions |
|
|
| ACP: main questions |
|
|
| Probes |
|
|
| Clinician | ||
| Lead-in questions |
|
|
| ACP: main questions |
|
|
| Probes |
|
|
Abbreviations: ACP, advance care planning; POLST, Physician Orders for Life-Sustaining Treatment.
Adjustments in wording were made between interviews.
We identified 5 major themes that represent the experiences of ACP for patients with decompensated cirrhosis, and these themes are described in detail herein. Patients expressed a willingness to engage in ACP in the outpatient setting, but patient engagement was not the practice of transplant teams. Discussions between transplant center clinicians and patients regarding prognosis did not stimulate the consideration of future health events or goals of care if transplant was unlikely, and these discussions were rarely helpful in preparing patients and their surrogate decision makers for end-of-life decisions. With the exception of social workers, most clinicians supported these conversations only near the end of life (Table 3).
Table 3. Major Themes and Representative Quotes From Interviews.
| Theme | Patient quotes | Clinician quotes |
|---|---|---|
| Theme 1: Most patient consideration of values, goals, and preferences occurred outside outpatient visits |
|
|
| Theme 2: Optimistic attitudes from transplant teams hindered the discussions about dying |
|
|
| Theme 3: Clinicians primarily discussed death as a strategy for encouraging behavioral change |
|
|
| Theme 4: Transplant teams avoided discussing nonaggressive treatment options with patients |
|
|
| Theme 5: Surrogate decision makers were unprepared for end-of-life decision-making |
|
Abbreviation: ICU, intensive care unit.
Theme 1: Most Patient Consideration of Values, Goals, and Preferences Occurred Outside Outpatient Visits
Patients reported thinking about or engaging in conversations with family members about their values and the type of care they would like to receive if they were close to dying. These sentiments often began around the time they became severely ill or hospitalized. Several patients expressed not wanting to prolong their life if they had “no hope” of recovery or if they were “living on machines.” Patients worried about being a burden on family or caregivers. They desired financial stability for their families and to minimize the emotional toll of their death. A few patients described their preferences regarding location of death or postmortem activities, such as cremation or burial processes.
Despite most patients being open to these conversations with continuity clinicians, few recalled having these discussions. Among the transplant team, only social workers reported consistently engaging patients and their caregivers about these topics. To open up the conversation, they asked questions such as “What’s really important to you?” and “What are you going to be comfortable with?” They also routinely encouraged patients to complete advance directives and to clarify surrogate decision makers. Other members of the transplant team would attempt to clarify decision makers and documentation only during acute hospitalizations but otherwise would not engage in deeper discussions.
Theme 2: Optimistic Attitudes From Transplant Teams Hindered the Discussions About Dying
Transplant center clinicians acknowledged the considerable uncertainty associated with prognoses and outcomes but did not use this uncertainty as an opportunity to explore patients’ goals and preferences for end-of-life care. When communicating prognosis, clinicians often used scores based on laboratory tests such as MELD-Na. For instance, at transplant centers, patients are encouraged to consider transplant as an option only after the MELD-Na score is 15 or higher given that the liver is unlikely to improve on its own after that point. To help patients understand the amount of time needed on the transplant waiting list, clinicians reported explaining to patients that higher MELD-Na scores were associated with shorter wait times.
Despite this preparation and regardless of transplant status, patients reported concerns about dying that often were left unaddressed. A few patients mentioned their frustration with being in limbo while either trying to get on the transplant waiting list or waiting for a new liver. Rather than exploring these sentiments, clinicians frequently encouraged patients and families to focus on optimistic outcomes, such as receiving a liver or striving for improved liver function and not needing a new liver. During transplant evaluation, the time was spent on educating patients about the benefits of a transplant, explaining the details of the procedure and need for immunosuppression, and instilling confidence and hope for a good outcome.
Transplant teams remained optimistic even as uncertainty grew, particularly for patients who were wait-listed or being evaluated for transplant. As patients on the waiting list became sicker, clinicians noted that the likelihood of dying and the likelihood of receiving a transplant were “50-50” but still maintained their hope for an organ. When patients were moved to deferred placement or taken off the waiting list, clinicians reported turning to ways that patients might overcome these barriers to get back on track. Strategies discussed by clinicians included managing addiction, mental health, or other social behaviors; obtaining more social support; addressing frailty or comorbidity; waiting to get sicker to be more competitive for an organ; or being evaluated at another transplant center. Even in situations when receiving an organ appeared far less likely than dying, clinicians almost always claimed that there “[were] still options” remaining. None of these situations ever provoked a conversation about patient goals or feelings about death.
Clinicians viewed their role as getting patients to transplant rather than preparing them for dying. Only when patients were no longer transplant candidates were clinicians less resistant to bringing up death, but it was often too late at this point, which a social worker indicated as “at the bitter end in the ICU.”
Theme 3: Clinicians Primarily Discussed Death as a Strategy for Encouraging Behavioral Change
In the few patients who reported that death was discussed by clinicians, they noted that the conversations were framed around trying to change patient behavior. Nearly all such discussions occurred during hospitalizations after patients were already seriously ill and often were triggered by an acute exacerbation. Patients recounted that clinicians brought up death to induce behavioral change or convince them of the need for a transplant. For example, patients recalled being told they that were “going to die without a transplant,” and those with alcohol-associated liver disease were told they “would die if they have anything [alcohol] ever to drink.” Several transplant center clinicians reported that such references to death were meant to convey the seriousness of the patient’s condition. Conversely, no patient or clinician described a discussion of prognosis or death during clinical stability (such as the initiation of transplant evaluation) that addressed patient goals, values, and preferences concerning end-of-life care.
Theme 4: Transplant Teams Avoided Discussing Nonaggressive Treatment Options With Patients
Only 1 patient reported sharing end-of-life wishes with a clinician, and transplant center clinicians acknowledged that such conversations were almost always initiated by patients and families. Because clinicians viewed nonaggressive care options, such as a referral to hospice or a do-not-resuscitate code status, as contradictory to the pursuit of transplant, they became frustrated when patients mentioned these topics. Rather than explore the motivation or conditionality behind these preferences, nearly all clinicians reported asking patients to choose between the goal of pursuing transplant and the goal of pursuing comfort-focused care. Social workers, despite their involvement, deferred to clinicians the discussions about prognosis and life-sustaining treatments.
Theme 5: Surrogate Decision Makers Were Unprepared for End-of-Life Decision-Making
Surrogate decision makers, who were frequently identified beforehand by patients, often participated in end-of-life discussions because patients were unable to meaningfully participate. Social workers and critical care physicians involved in these discussions noticed that surrogates were unprepared for the news that a transplant was no longer a realistic option. This situation made it challenging for all parties to discuss decisions about withdrawing life-sustaining treatments and arranging disposition. Other members of the transplant team were encouraged to help surrogates understand the prognosis. Critical care physicians also stated that traditional forms of end-of-life care, such as home hospice, often were not the best options for these patients at the end of life given the level of support they would need at home from caregivers.
Discussion
In this multicenter qualitative study, we found substantial deficits in ACP for patients with decompensated cirrhosis. Patients reported infrequent conversations with transplant center clinicians about death and dying. Clinicians used the prospect of death, often couched in a numerical prognostic estimate, as an opportunity to introduce the need for a transplant but not to explore patient fears and preferences. As patients became sicker, the focus on transplant continued to overshadow the need for end-of-life decision-making. Despite patient interest, such conversations were deferred until episodes of clinical decompensation occurred in the inpatient setting. At the end of life, surrogate decision makers struggled with choosing among the limited options presented to them.
Clinicians focus on maintaining hope and keeping the option of a transplant open for patients, even as the probability of successfully reaching this goal becomes smaller. Although patients prefer prognostic communication that presents a range of care options and possibilities,28,29 the opportunity to provide a highly successful treatment in transplant makes communication uniquely challenging for clinicians, which has been suggested in a previous qualitative study.15 The uncertainty of a prognosis provides clinicians a chance to counsel patients on the trade-offs required in continuing aggressive care and to elicit a patient’s values and goals in preparation for less fortunate outcomes, but such topics are avoided, although patients view such conversations favorably.30 Social workers, although motivated to have these discussions, received little support from other members of the transplant team to frame these possibilities and decisions.
Another opportunity to explore patient goals and values comes when patients report preferences for care that appear contradictory, such as desiring both hospice and transplant. Instead of examining this preference, clinicians in this study reported pressuring patients to choose either transplant or comfort, but not both. Instead, nuanced conversations that link treatment goals to likely outcomes could ensure that end-of-life care is goal-concordant.31 Models of communication that incorporate discussions about preferences for care in future health states if transplant is impossible or unsuccessful can be merged with current communication patterns without disrupting the goal of achieving transplant. Rather than implementing informal transplant center policies (eg, all patients on the waiting list should be full code32), clinicians could improve how they handle such conversations.33
Previous studies have reported poor prognostic awareness among patients with decompensated cirrhosis as well as high rates of life-sustaining treatment use, low rates of hospice utilization, and poor quality of end-of-life care among patients who are both considered and not considered for transplant.2,4,34,35,36,37 The present study suggests that shortcomings in how transplant teams communicate patient prognosis and incorporate patient values and goals into end-of-life decision-making delay the provision of high-quality palliative care at the end of life. To modify this pattern, health care systems in which these patients are treated must be as intentional and prepared in addressing end-of-life experiences as in offering maximally aggressive therapy. Policies, practice guidelines, and quality improvement initiatives that focus on reducing patient and clinician barriers to ACP conversations and integrating specialty palliative care services may help achieve this goal.
Clinicians should ensure that the care provided to all patients, particularly those with a serious illness, is consistent with patient values, goals, and preferences. Conducting ACP conversations is supported by reports such as Dying in America38 as well as subspecialty societies that guide the treatment of patients with advanced cancer,39 heart failure,40 dementia,41 chronic obstructive pulmonary disease,42 and chronic kidney disease,43 although not yet by any subspecialty organizations for patients with liver disease. Intervention is needed for ACP to become the standard practice for patients with decompensated cirrhosis.
Strengths and Limitations
This study has several strengths. To our knowledge, it is the first qualitative study to provide an in-depth description of the specific behaviors associated with ACP as reported in face-to-face interviews by clinicians and patients with decompensated cirrhosis, behaviors that were described only in surveys in previous studies.33,44 Perspectives from several types of clinicians contributed to the richness of the data, in addition to sampling from 3 different transplant centers. We also used triangulation between patient and clinician transcripts, member checks, and peer debriefing to ensure the trustworthiness of our analysis.
This study also has limitations. We did not capture the perspectives of all informants involved in ACP, including specialty palliative care teams and primary care physicians. However, we believe the information provides a rich understanding of how ACP is framed at transplant centers. Because this was a qualitative study, we were unable to present the frequencies of these behaviors. However, we believe that similar findings in different clinician groups is reassuring. Practices at the transplant centers in this study may not necessarily reflect those at transplant centers elsewhere, yet we believe the results of this study will resonate with others who care for patients with decompensated cirrhosis at the end of life. In addition, the experiences at transplant centers may not reflect the experiences of centers that do not offer transplant. However, clinicians at transplant centers have reported being more comfortable with ACP discussions than community-based clinicians,33 which suggests a need for improvement at these centers as well, although the barriers may be different.
Conclusions
This qualitative study found that patients with decompensated cirrhosis had inadequate ACP throughout their illness until the end of life. Transplant center clinicians infrequently engaged patients in conversations about death and dying as well as about values, goals, and preferences regarding end-of-life care. This finding may partly explain the aggressive life-sustaining treatment provided to patients at the end of life.
eTable. Characteristics of Transplant Centers Included in Study
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Associated Data
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Supplementary Materials
eTable. Characteristics of Transplant Centers Included in Study