A Qualitative Study of Pulmonary and Palliative Care Clinician Perspectives on Early Palliative Care in Chronic Obstructive Pulmonary Disease

Abstract

Background:

Guidelines recommend that pulmonary clinicians involve palliative care in chronic obstructive pulmonary disease (COPD); however, integration before advanced stage, that is, early palliative care, is rare.

Objective:

To explore and compare pulmonary and palliative care clinician perspectives on barriers, facilitators, and potential referral criteria for early palliative care in COPD.

Design:

Qualitative descriptive formative evaluation study.

Setting/Subjects:

Pulmonary and palliative care clinicians at a tertiary academic medical center.

Measurements:

Transcribed interviews were thematically analyzed by specialty to identify within- and across-specialty perspectives on barriers, facilitators, and referral criteria.

Results:

Twelve clinicians (n = 6 pulmonary, n = 6 palliative care) participated. Clinicians from both specialties agreed that early palliative care could add value to disease-focused COPD care. Perspectives on many barriers and facilitators were shared between specialties along broad educational, clinical, and operational categories. Pulmonary and palliative care clinicians shared concerns about the misconception that palliative care was synonymous to end-of-life care. Pulmonologists were particularly concerned about the potential risks of opioids and benzodiazepines in COPD. Both specialties stressed the need for clearly defined roles, consensus referral criteria, and novel delivery models. Although no single referral criterion was discussed by all, frequent hospitalizations and emotional symptoms were raised by most across disciplines. Multimorbidity and poor prognosis were discussed only by palliative care clinicians, whereas medication adherence was discussed only by pulmonary clinicians.

Conclusions:

Pulmonary and palliative care clinicians supported early palliative care in COPD. Continued needs include addressing pulmonologists' misconceptions of palliative care, establishing consensus referral criteria, and implementing novel early palliative care models.

Introduction

Chronic obstructive pulmonary disease (COPD) affects 15 million Americans and is the fourth leading cause of death in the United States.¹ International guidelines from the Global Initiative for Chronic Obstructive Lung Disease call for integration of palliative care for symptom relief in advanced COPD but do not provide guidance regarding the role of palliative care for COPD patients and their family caregivers before end stage, that is, early palliative care.² Descriptive studies demonstrate that COPD patients and their family caregivers have significant palliative care needs before the disease progresses to more advanced stages, yet rarely receive timely palliative care.^3–6 Thus, individuals with COPD seldom have access to its demonstrated benefits until end-of-life nears.^7–9

There are limited data on barriers and facilitators to implementing early palliative care in COPD from the perspective of clinicians across disciplines.^10–12 Existing data have mainly been drawn from European clinician samples where single-payer health care systems differ greatly compared with the United States.¹³ Although some have used the phrase “early palliative care,” studies focus predominately on end-stage COPD.¹⁴ Data have also demonstrated that pulmonary clinicians support palliative care in COPD; however, there is a lack of consensus on the appropriate timing to introduce palliative care.^15–17

Within a broader framework for intervention development, we compared pulmonary and palliative care clinicians' perspectives on barriers, facilitators, and potential referral criteria for early palliative care in COPD. We wanted to understand how the two disciplines perceive early palliative care in COPD to guide the development of an early palliative care program that would be acceptable and relevant to COPD patients and clinicians across specialties.

Methods

Design

We conducted a qualitative descriptive formative evaluation study using the Medical Research Council Framework for the Development of Complex Interventions to develop an early palliative care intervention in COPD.^18–22 We recruited a purposive sample of pulmonary and palliative care clinicians (physicians and nurse practitioners) between March 2017 and August 2017 from the University of Alabama at Birmingham (UAB), the largest tertiary referral center in Alabama serving urban and rural areas.²² The interviewer, a male pulmonologist and experienced qualitative researcher, conducted individual, semi-structured interviews in participants' private offices.

Semi-structured interviews

We conducted interviews using an interview guide based on literature review and our previous research (Table 1).^5,19,23 We sought participant responses to a standardized definition of early palliative care from National Consensus Project guidelines.^5,24 Following this, we explored pulmonary and palliative care clinicians' perspectives on barriers, facilitators, and potential referral criteria for early palliative care in COPD. We employed member checking by asking participants their perspectives on what previous participants had said (e.g., “Other participants have said X. What do you think about that?”). We adhered to Consolidated Criteria for Reporting Qualitative Studies guidelines for reporting qualitative studies.²⁵ The UAB Institutional Review Board approved the study. Given the study's low risk, clinician participants provided verbal informed consent after being provided an information sheet.

Table 1.

Interview Guide Domains and Sample Questions

Domain	Questions
Early palliative care in COPD	Early palliative care has been defined in the following way: “Specialized medical care that provides physical, emotional, spiritual, and social support alongside outlook planning for COPD patients and their family caregivers, offers a layer support to improve quality of life, and is appropriate at any stage of illness concurrent with standard medical treatment.”
Early palliative care in COPD	What are your first thoughts about this definition?
Barriers to early palliative care in COPD	What are challenges you see to bringing early palliative care for patients with COPD?
Facilitators of early palliative care	What are some ways that you see could help bring early palliative care to COPD?
Referral criteria	Can you think of potential referral criteria for early palliative care in COPD?
Referral criteria	Prompt: When should a COPD patient be referred to palliative care?

COPD, chronic obstructive pulmonary disease.

Data analysis

All interviews were audio-recorded and transcribed verbatim by a professional transcription service. Using NVivo Software (QSR International), the PI (A.S.I.) open coded the transcripts concurrent with the interviews, developed a preliminary list of codes related to the research questions, and reviewed the codes with another member of the study team (M.A.B., a leading expert in qualitative research in palliative care). Two members of the study team (A.S.I. and M.A.B.) used constant comparison to refine the codebook and developed multiple themes through iterative discussions and frequent meetings.²⁶ We identified themes by participant, grouped themes into broader categories, and compared perspectives on barriers, facilitators, and referral criteria between specialties. We reached thematic saturation at 10 clinicians and recruited two additional participants to confirm this conclusion. Determination of thematic saturation was guided by theoretical and inductive approaches, operationally defined as the point at which interview revealed no new codes or themes relative to previous interviews.^21,22,27

Results

We recruited 12 clinicians (n = 6 pulmonary and n = 6 palliative care) (Table 2). Ten (83.3%) participants were physicians, and two (16.7%) were nurse practitioners. Interviews lasted on average 52 minutes (range 34–72). After being provided a standardized definition of early palliative care, all participants believed there was a potential value for early introduction of palliative care to augment comprehensive COPD care for patients.

Table 2.

Participant Characteristics (n = 12)

	n (%) or mean ± SD
Specialty
Pulmonary-critical care (CLIN 001, 002, 007, 010, 011, 012)	6 (50.0)
Palliative care (CLIN 003, 004, 005, 006, 008, 009)	6 (50.0)
Age (years)	45.9 ± 15.4
Race (white)	11 (91.7)
Gender (male)	9 (75.0)
Discipline
Physician	10 (83.3)
Nurse practitioner	2 (16.7)
Academic rank
Fellow	1 (8.3)
Instructor	2 (16.7)
Assistant professor	5 (41.7)
Associate professor	3 (11.5)
Professor	1 (3.8)

SD, standard deviation.

Barriers to early palliative care in COPD

Several themes of barriers to early palliative care in COPD emerged within broad educational, clinical, and operational categories (Table 3). Within the category of educational barriers, a common theme was “misconceptions of palliative care.” Many pulmonary clinicians viewed palliative care as tantamount to end-of-life care and even interchanged the words “palliative care” and “hospice,” whereas some pulmonologists recognized the misconceptions from within their own specialty. Some pulmonary clinicians reflected beliefs that palliative care could provide comprehensive symptom management to improve quality of life before the end of life, whereas others believed palliative care was strictly end-of-life care. In comparison, multiple palliative care clinicians expressed beliefs that these misconceptions could stem from a public misunderstanding of the term “palliative care,” which in turn manifested in what COPD patients believe.

Table 3.

Pulmonary and Palliative Care Clinicians Perspectives on Barriers to Early Palliative Care in Chronic Obstructive Pulmonary Disease

Themes	Exemplary quotes
Themes	Pulmonary (n = 6)	Palliative care (n = 6)
Educational barriers
-Misconceptions of palliative care -Goes against pulmonary-critical care training	“I largely see it as providing care and comfort in the advanced stages of disease.” (CLIN001). “I think that where palliative care is the most effective is getting the patient stabilized for a home mediated death, or in a facility mediated death for palliation, for end of life.” (CLIN002). “Palliative care doesn't mean not doing anything, because I think that's what some people think of palliative care. ‘We're not gonna do anything but give them medicine to make them comfortable.’” (CLIN010) “I think that when patients go to hospice, they think death. If you said “hospice,” they would be very against that. I think the term “hospice” is offensive. I think “palliative” is not as offensive, but probably is in the middle. I think supportive care is probably the best way to introduce a comfort-based approach to care if you're bringing that up for a patient. I think when a patient hears ‘hospice,’ their first thought is, ‘Well, this is it.’ I think that palliative care is, ‘We can't fix your problem, but we can manage the manifestations of your problems or your symptoms.’ The thing that I hear over and over is it's giving up.” (CLIN012) “I feel like there's still that negative connotation of what palliative care does. I think palliative care is still thought of as end-of-life care. That's not what they do. They can exponentially improve quality of life. They may even improve quantity of life.” (CLIN011) “I think pulmonary patients are fighters you know. They've already been intubated, and they view themselves as, ‘I probably already should be dead, right?’ I think our patients' views of true palliative care and hospice—it would be a rare circumstance that they're really on board with that.” (CLIN002) “Critical care people want to keep people alive no matter what. They feel like they're abandoning their patient if they don't keep them alive even to the point of cruel and unusual punishment for the patient, and the family sometimes sees that. It's just awful for them. That's almost the opposite of what they've been trained to do—snatch people from the jaws of death all the time.” (CLIN007)	“All hospice is palliative care, but not all palliative care is hospice. I would say, ‘I'm not sending you to them because I think you're gonna die in the next six months. That's hospice. I think you've got a serious illness, and I'm worried where it's headed.’” (CLIN009) “I wonder if that is still something that is not educated very well from our field to others. The fact that hospice does not equal palliative care is still something that we need to work on.” (CLIN004) “They could either call it palliative care or supportive care. What sometimes happened is we would show up and there was a lot of confusion about who we were—families felt like we were social work. It actually caused more confusion. What palliative care is, and where the word comes from, it's actually a really lovely image. The idea of cloaking someone or covering someone from the suffering of illness. There's nothing about death in that.” (CLIN003) “It's kind of self-fulfilled. Pulmonologists consult late, so we see their patients at the end of life. I think if we could help them say, ‘Let's consult earlier and see what happens,’ they're going to see that we're not just making everyone DNR and putting them on morphine, and they're dying. They're going to see the more upstream approach of what we do. The more they can see that, the more they'll go, ‘Oh, they're not just the end-of-life cloaks and sickle kind of team. They can actually help much more upstream.’” (CLIN005)
Clinical barriers
- Fears of opioids and benzodiazepines for symptom management in COPD - Unclear timing of early palliative care - Prognosticating in COPD is difficult	“We always equate that anxiety from dyspnea. We rarely give benzos in a lung disease patient. It's a very effective method in treating their anxiety. That's one of the things that we have always avoided doing in people who have chronic respiratory failure.” (CLIN011) “The thing I have to be careful about when I call hospice is they love to give drugs, and they love to give people lots of narcotics. I don't want these people to have lots of narcotics if I think they have mobility problems, and they need help, and the family needs the help. I don't want them to be over-sedated and die because they weren't ready to die. Many hospice nurses don't separate palliative care for COPD versus palliative care for a cancer patient. There's a difference. Palliative care for a COPD patient is relieving their symptoms of dyspnea, which is usually their big problem. People just are so short of breath. I want to relieve their dyspnea, but I don't want to kill them or over sedate them. Someone with cancer may not have a respiratory arrest with a certain amount of narcotic, but the COPD patient may get enough of a suppression that they drop their oxygen saturation and have an arrest.” (CLIN010) “I think it's certainly worth exploring, and I think with healthy communication and discussion, we can probably define our rationale for limiting or avoiding certain kinds of interventions where possible. If the intent is hospice referral, we've probably missed the opportunity for palliative to at least have some effect on some of these patients, but I guess honestly where that line is I'm not sure I can accurately define it.” (CLIN001) “With COPD, we've noticed that you don't really know. Basically, it's not as clear-cut, because we really can't predict how long they're going to live and how well they're going to do. There are people who have an FEV₁ of less than 1 liter, and they go forever.” (CLIN010) “It's not necessarily an end-of-life thing, so that's not the issue. The issue is when do the needs of the patient get to the point that the hospice people—I mean, the palliative care people—are more likely to help than any?” (CLIN007) “This is probably a function of education on my part as to how beneficial early intervention might be for those patients. I think if it seemed to make a difference, I'd certainly support it.” (CLIN001)	“It's the same reason that people are afraid that if, ‘I go on hospice they're just going to put me on a morphine drip and I'm going to die.’ Well, there's some truth in that. Unfortunately, a rotten apple spoils the bunch. If you're a referring physician, and you send one of your COPD patients, and the next thing you know, they're snowed on benzos and they have an event, I sure as hell would think twice about consulting again.” (CLIN003) “The first thought a palliative care physician has is opioids, and that is another reason that pulmonologists are terrified to consult us, too. They think we're just going to ‘narc’ up their patients.” (CLIN005) “One of the most common barriers we see is clinicians, especially those in training, usually are very fearful of using opioids and benzos for dyspnea with fear of causing decompensation from a respiratory standpoint. We try to educate as much as we can. When you do it appropriately and start at appropriate doses, that is not the case. That's a huge barrier.” (CLIN004) “One of the challenges that I think we struggle with and don't have an evidence base sufficient to guide us at this time is kind of balancing the symptom management medications that we use with the potential impact of those medications on respiratory function or longevity.” (CLIN006) “I think the tough thing with COPD is that prognostication can sometimes be difficult. Some people say, ‘Oh, they're on oxygen now, it's end stage COPD,’ but that's not necessarily the case. They could live years in that state. Then, I've seen folks at the end of their life with COPD. I think the biggest question I usually get from patients is usually, ‘Am I going to suffocate to death?’” (CLIN004) “I would say COPD and congestive heart failure are very similar to me in my experience because COPD is such a chronic disease that tends to be a revolving door in and out of the hospital. They have exacerbations. They're critically ill, and a lot of times they bounce right back. One of the challenges I think is figuring out when do you get involved, when do we see them first, and how we develop that relationship over time.” (CLIN 005)
Operational barriers
- Insufficient time to provide early palliative care in clinic - Inadequate reimbursement for palliative care - Limited palliative care access and workforce shortage	“A lot of the older patients, especially with advanced COPD, don't mind coming for a 3 or 4-hour doctor visit, but the doctor ain't got time for the 3- or 4-hour doctor visits, right?” (CLIN002) “A lot of it's just time in clinic. When you've got a busy clinic, it's hard to focus on that and have a prolonged discussion.” (CLIN001) “In a perfect world, if you had the money for palliative care, fine.” (CLIN002)	“I think the reflexive answer everyone says is time. I get frustrated with that answer. The reality is, we're never gonna have more time. We can keep sitting and stomping our feet and saying we just need more time or we need longer appointments. Time is not the magic answer. It's how do we use that time more efficiently? How do we really collaborate? How do we really share a care plan? How do we trust each other's roles and each expertise? I think those are the challenges.” (CLIN003) “It's hard to bill for, you know. Those sorts of conversations, even under the new Medicare coding and billing criteria around advanced care planning, I don't know that you could count those.” (CLIN006) “There are market restrictions on hospice services for COPD, which limits things quite a bit. We don't always have good solutions about what kind of programs or services to offer them.” (CLIN008) “The reality is, when you think of all the patients with COPD, there's probably not enough of us to see all those patients. (CLIN009) “There will never be enough palliative care clinicians. We have barely enough to do our inpatient work. When you're limited to inpatient, you see palliative care at the end of life. You don't get enough early palliative care. In order to see palliative care more upstream, you have to move it outpatient. That's been a challenge to grow a group of clinicians to be able to see enough outpatient.” (CLIN005)

DNR, do not resuscitate; FEV₁, forced expiratory volume in 1 second.

Themes within the category of clinical barriers centered on concerns about symptom management in COPD, particularly the management of dyspnea with opioids and benzodiazepines. Pulmonary clinicians expressed serious concerns that palliative care clinicians would be quick to prescribe these medications to COPD patients, and this concern hindered their referral to specialty palliative care. Likewise, palliative care clinicians recognized this as a potential barrier to referral for COPD patients. A second major theme in this category centered around unclear timing and was a shared concern among pulmonary and palliative care clinicians. Pulmonary clinicians seemed supportive of early palliative care but were unsure when to refer. Palliative care clinicians also raised concerns about how to frame a palliative approach and have early discussions about preferences for end of life in the setting of an unpredictable illness trajectory with frequent hospitalizations (Table 3).

Themes within the category of operational barriers focused on practical considerations to integrating early palliative care in the ambulatory setting. Pulmonary and palliative care clinicians were concerned about whether ambulatory palliative care clinics could handle a large influx of COPD patients who may need palliative care if referral were to increase. Clinicians from both disciplines shared concerns about insufficient time in clinic to conduct comprehensive palliative care for patients, palliative care workforce shortages, and the low financial reimbursement for pulmonologists who might integrate a primary palliative care approach within their practice (Table 3).

Facilitators of early palliative care in COPD

Table 4 compares multidisciplinary perspectives on potential facilitators for early palliative care in COPD. Themes on facilitators for early palliative care were also organized into broad educational, clinical, and operational categories. Within the category of educational facilitators, pulmonary and palliative care clinicians emphasized the need for clearer role definition from the onset of referral and improved education in primary palliative care in pulmonary medicine. Clinical facilitators included the development of consensus referral criteria and more training in how to prognosticate based on COPD patients' values and preferences. Finally, both disciplines described potential operational facilitators focused on novel delivery models such as nurse-led, telehealth, home-based, and embedded programs where palliative care clinicians see patients in pulmonary clinic (Table 4).

Table 4.

Pulmonary and Palliative Care Clinician Perspectives on Facilitators of Early Palliative Care in Chronic Obstructive Pulmonary Disease

Themes	Exemplary quotes
Themes	Pulmonary (n = 6)	Palliative care (n = 6)
Educational facilitators
- Clearly define palliative care for pulmonologists - Train pulmonologists in primary palliative care	“You have to teach people that are taking care of patients like this. Pulmonologists are many times well-meaning in palliative care. They want to make people comfortable. They want to make it where people are okay, but they're not really trained in the psyche of understanding how to make people feel good. That ought to be part of a training program.” (CLIN010) “I think there's a role for getting a better understanding from our side on symptom management and palliative care. To supplant the service itself, I think that would be a mistake.” (CLIN011)	“It makes more sense, in some ways, to have someone who's trained within. That person knows the culture, they're known, and they know the language. It makes more sense. Then the question is can they add that skill?” (CLIN003) “I think that where the field is going is teaching subspecialty providers to have basic skills in symptom management and initiating advanced care planning. That's something that needs to happen earlier on, not just at the end of life.” (CLIN004) “If you have ovarian cancer, you see palliative care. It's just part of what they do. They don't want for you to have advanced ovarian cancer. ‘I feel like having that sort of thing introduced at the outset of care like,’ ‘We have this team, they're part of the care that we provide to our patients. We consider it to be a very important part of our team. At some point in the future, I'll ask you to see them. Usually that happens when we're having difficulty with symptoms. You could ask me to see them at any point that you feel it might be helpful.’” (CLIN006)
Clinical facilitators
- Develop early values-based prognostication - Develop consensus on referral criteria - Involve family caregivers	“You knew they weren't gonna live very long. You knew that they had a limited life expectancy, and sometimes, and you could correlate it by—BODE index is maybe the best, but FEV₁ can correlate it very nicely in terms of once it gets below certain numbers. Not everybody's gonna die, but you can say that the statistical probability is that they're gonna die, and there's gonna be a curve within six months or a year or whatever.” (CLIN007) “I think in COPD, the caregiver, especially if you have a very elderly patient is very crucial.” (CLIN002)	“Nobody explores with them what's important in their life, and what they're going to lose in their life if their disease progresses, or when their disease progresses.” (CLIN009) “A great way of prognosticating is to acknowledge uncertainty, to acknowledge what we don't know.” (CLIN003) “I don't feel as strongly that there ought to be automated triggers. Thinking thoughtfully about the sorts of things in this population that are markers for anticipated mortality.” (CLIN006)
Operational facilitators
- Increase the number and type of palliative care providers - Develop more flexible models of palliative care: Telehealth, home-based, pulmonary care clinic-embedded palliative care	“I think it would be nice to have an in-house palliative care nurse or assign that to maybe one of the COPD nurses and say, we're gonna train you to identify factors that are either palliative care or things we can do that are palliative care-like without full-blown palliative care. Palliative care doesn't have to be an on or off switch.” (CLIN010) “If a nurse practitioner would do this, you get one of our nurse practitioners and add this to her role. It's not like she's gonna be seeing 20 patients a day. She may see two a week.” (CLIN010)	“Quite honestly, one of the most effective clinical encounters that I have seen this year is a home visit. I know that would be technically probably hard to do, but I think that's a setting in which patients always really appreciate it. Family members always really appreciate it.” (CLIN004) “The other thing we're looking at is can we incorporate telemedicine, being able to be in more places and use our expertise more efficiently and more widely as a consultant or doing home visits via iPad.” (CLIN005) “Could you have an advance care planning champion within clinic who has a separate room and only does a couple in an afternoon?” (CLIN005) “We need a system where somebody's nose is not to the grindstone, and can get an overall view and say, okay, let's educate the patient on what's coming. We just need a bigger picture.” (CLIN009) “I think we want to include our interprofessional colleagues. I wish that I could round with the psychologist. If I had a psychologist that I could just take with me everywhere, I think all the care I provided would be better. Our chaplains, I think addressing those issues in terms of—and I believe wholeheartedly that those things work. Relaxation things, mindfulness, CBT around fixed ideas. Really working with people to help them cope with anxiety. Those things work.” (CLIN003)

CBT, cognitive behavioral therapy.

Potential referral criteria for early palliative care in COPD

As given in Table 5, pulmonary and palliative care clinicians shared several priority referral criteria for early palliative care in COPD. Although no single referral criterion was discussed by all, frequent hospitalizations and emotional symptoms were discussed by many clinicians from both disciplines. Other shared priority referral criteria included poor nutritional status, declining functional status, severe dyspnea, and continuous oxygen. Multimorbidity and poor prognosis were discussed as potential criteria by only palliative care clinicians, whereas medication adherence was only discussed by pulmonary clinicians.

Table 5.

Pulmonary and Palliative Care Clinician Perspectives on Referral Criteria for Early Palliative Care in Chronic Obstructive Pulmonary Disease

Themes	Exemplary quotes
Themes	Pulmonary (n = 6)	Palliative care (n = 6)
Frequent hospitalizations and ICU admissions	“The red flags are frequent hospitalizations. They keep having exacerbations. They have a lot of hospitalizations, but they shouldn't be because based on their numbers. They cannot stay out of the hospital.” (CLIN010)	“The mortality of people with COPD who've been hospitalized for an exacerbation is very high. If you have two or three hospitalizations, it gets higher.” (CLIN007) “Is it number of hospitalizations or emergency department visits or number of exacerbations in a year? I mean, that could be more upstream, right? (CLIN005) “Recurrent hospitalizations is usually good target. Anybody who's had to be ventilated I think is definitely a point. If your COPD is bad enough that you've had to be on a ventilator, then the pretest probability of being on it again is much higher than someone who might have severe disease but never had any respiratory failure. I think having had to receive mechanical ventilation, recurrent hospitalizations, whether you want to say twice in a couple months or three times a year, whatever number you want. Those are probably folks that might benefit.” (CLIN008) “I think when they get admitted to the ICU for COPD, if that's the primary driver of pushing them into the ICU. No longer are we just sort of dabbling with early COPD. Now something's changed to the point where you may get the patient's attention, you may get the wife's attention, you may get the child's attention, the people in their life to go, ‘Oh, this was scary. We thought papa was going to die.’ I think that could be a sentinel event, you know? Now, that's pretty upstream.” (CLIN009)
Emotional symptoms	“I think we also see a fair amount of anxiety in part related to the distress with breathing but in part related to the unknown about what to expect. They've either had emotional support or some control over anxiety, depression, and so forth, and there may have been some other associated symptoms, not necessarily shortness of breath, but things I don't necessarily pick up in clinic that somebody with palliative skills might and address those kinds of things.” (CLIN001) “It's been described that anxiety and depression, especially if left untreated, does co-associate with poor health outcomes.” (CLIN002)	“In general, the thing that I find undermanaged or under-addressed in this population is anxiety. If there was a way to screen for depression and anxiety symptoms, I would certainly use that as a trigger.” (CLIN 006) “I think if anxiety or depression is something that's seen earlier in the disease, perhaps it could be helpful.” (CLIN004)
Severe airflow obstruction/marked reduction in lung function	“Pulmonary function tests obviously will help. Severe disease by FEV₁.” (CLIN010)	“Certainly the most objective findings would be a marked reduction in FEV₁ or severe obstructive pattern on PFTs. I think there has to be those findings, plus symptom burden, and impact on quality of life.”
Poor nutritional status/cachexia	“If you have a patient with declining nutritional status with a pulmonary disease, it's bad news, right?” (CLIN002) “Cachexia, obviously cachexia is a good trigger.” (CLIN007)	“If you're not meaning to lose weight because of your COPD, but you're losing weight, there are some body systems failing. Unintentional weight loss is a big thing, an ‘uh-oh’ diagnosis for me. That really gets my attention.” (CLIN 009) “I see a lot of pulmonary cachexia and deconditioning, symptoms with early satiety and constipation related to the other medications that they're on.” (CLIN008)
Declining functional status	“I think bigger-picture, functional status-based prognostication tends to be the best in the long run. Really looking at how functional this person, how far can they walk, and how are they eating. If those things are dropping off, to me that's a really important sign.” (CLIN010) “I guess the ones that come to mind are symptom management. When patients have become less functional and we've maximized their COPD therapy. They're on oxygen, a good spectrum of bronchodilator therapy, chronic corticosteroids, and still just not able to function well or have various complaints. Deconditioning, a big factor. Loss of exercise ability.” (CLIN001)	“Predominantly it's the getting worse and not knowing what to expect and needing more care, but not wanting to ask for it.” (CLIN008)
Severe dyspnea	“I think unremitting breathlessness. That is a good predictor of death in COPD patients, no matter what the pulmonary functions or anything else showed.” (CLIN010) “Some people with an FEV₁ of 50%-predicted might actually feel like they have decent quality, and their shortness of breath may not be severe to the point where they're on oxygen. On the other hand, some people could have an FEV₁ of 50%-predicted and are on oxygen but have severe symptoms.” (CLIN011)	“We could push it upstream to the point where they start having a functional decline from dyspnea. Maybe not even hypoxia, but just dyspnea.” (CLIN009) Symptom burden, dyspnea that can't be palliated with optimizing beta-2's and anticholinergics.” (CLIN008)
Need for supplemental oxygen and noninvasive ventilation	“How much supportive devices or care are they needing? Do they need oxygen or BiPAP at night and for naps during the day? Do they need it continuously? Maybe how that's affecting their quality of life. Some people can live on BiPAP 24 hours a day, and they're okay with that. Then, some people, that's not okay.” (CLIN012)	“I think it's probably a good conversation to have once they qualify for home oxygen or continuous oxygen.” (CLIN004)
Multimorbidity		“If they're a multimorbidity patient, not just COPD, but they have heart failure or just other chronic diseases, that could be an identifier for worse prognosis, and so therefore maybe better to get us involved.” (CLIN004)
Lack of adherence to medical regimen	“I would say unexplained compliance with medications. Lack of compliance oftentimes signals they have mental health issues.” (CLIN002)“Somebody notices they're not adhering to their medicines. Those people ought to be considered for somebody to hawk them to really stay on top of them. You're using palliative care or hospice to hawk people to make them more compliant so they don't keep failing.” (CLIN010)
Poor prognosis measured by surprise question		“A surprise question, wouldn't be surprised if the person died in the next year, is a good thought.” (CLIN008)“Any patient that falls in that category of, ‘We would not be surprised if they die in the next year.’ That's a different question than, ‘Are they likely to die?’ This is, would you be surprised if when you evaluate all the data and come up with a gestalt impression, would you be surprised. If you go, ‘Hmm, no, I would not be surprised if this patient dies in the next year.’” (CLIN009)
Challenging family dynamics		“I would say the criteria is similar to those that we use for cancer patients. Challenging family dynamics. Challenging care decisions. Where they're having to balance healthcare priorities that don't all fall within the scope of expertise of a pulmonologist.” (CLIN006)
Other symptoms	“I think if you're requiring a lot of pain medication, requiring a lot of anti-emetics, that could trigger maybe there needs to be a little help.” (CLIN010)

ICU, intensive care unit; PFTs, pulmonary function tests.

Discussion

We conducted a qualitative descriptive study to elicit pulmonary and palliative care clinicians' (n = 12) perspectives on early palliative care in COPD, including barriers, facilitators, and referral criteria. This multidisciplinary cohort agreed in principle that early palliative care could be beneficial for patients with COPD. However, participants shared several educational, clinical, and operational barriers that would need to be addressed to improve early palliative care access and delivery in COPD. The most important were educational barriers on misconceptions of the role of palliative care, clinical barriers to comprehensive symptom management, particularly using benzodiazepines and opioids in COPD, outlook planning in the setting of an unpredictable illness trajectory, and workforce limitations. Potential referral criteria for early palliative care described by clinicians spanned both pulmonary and nonpulmonary domains, with frequent hospitalizations and emotional symptoms shared as high priority referral criteria between disciplines. The results from this study can guide development of acceptable early palliative care programs and interventions for COPD patients and their family caregivers that cross both disciplines.

Findings from this study are consistent with national data on barriers to implementation of palliative care in serious illness. Aldridge et al. identified barriers to implementation of specialist palliative care along education, implementation, and policy domains.²⁸ Educational efforts on palliative care for clinicians caring for COPD patients may dispel the misconception that palliative care is only equivalent to end-of-life care. This theme was frequently described by pulmonary clinicians in our cohort and may in part be owing to pulmonologists' experiences as intensivists who often interact with a palliative care team at a patient's end of life in the intensive care unit. However, there may be a potential role for consistent primary palliative care education integrated into the training curriculum for pulmonary clinicians and applicable to the ambulatory setting. Several formal programs in primary palliative care exist in the United States.²⁹ To reach a broad audience of pulmonologists, organizations such as the American Thoracic Society and the American College of Chest Physicians may wish to invest in the development, dissemination, and assessment of impact of these educational programs.

A priority clinical barrier that emerged in our study centered on comprehensive symptom management in COPD, particularly the perceived tension on the part of pulmonologists toward the role of opioids and benzodiazepines in COPD. This major barrier to holistic management of dyspnea and emotional symptoms in COPD has persisted for the past decade, and fears of using these medications in COPD have been echoed by patients, caregivers, and clinicians from multiple disciplines, including general practitioners and respiratory therapists.^30–33 Refractory dyspnea and severe anxiety symptoms in COPD can be more severe than those experienced in advanced cancer and could serve as ideal triggers for palliative care.³⁴ However, pulmonary clinicians in our study expressed a fear of overmedication with opioids and benzodiazepines leading to potential respiratory suppression in chronic respiratory failure. Previous data reveal only moderate quality of evidence in support of opioids for dyspnea in COPD,³⁵ whereas retrospective and case–control studies highlight potential adverse events when benzodiazepines and opioids are used in older adults with COPD,^36,37 which likely contribute to the concerns raised by pulmonologists in our study. Opioids are commonly used in the palliation of refractory dyspnea, and mixed methods research data in small samples support its potential benefits in COPD.³⁸ Although awaiting a prospective clinical trial on opioids in the relief of refractory dyspnea in COPD, collaborative efforts between pulmonary and palliative care clinicians are needed to address this clinical dilemma to balance dyspnea relief with the potential for respiratory suppression in COPD.

Working with patients and their family caregivers to develop prognostic awareness before the end of life is a pinnacle of early palliative care that has been associated with improved quality of care in COPD.^39,40 Palliative care clinicians in our cohort acknowledged the importance of having early value-based discussions in COPD. However, advanced care planning is rare in patients with chronic respiratory diseases.⁴¹ Clinicians from both disciplines in our cohort noted a lack of consensus referral criteria and an unpredictable illness trajectory as major barriers to having proactive discussions about end-of-life care in COPD. Our data push forward the research on this topic and can be used to guide timing of early outlook planning in COPD. For instance, clinicians in our cohort acknowledged the potential disconnect between severity of airflow limitation on spirometry and symptom burden. COPD patients may suffer from high symptom burden regardless of the severity of airflow limitation, so it would be important to routinely measure symptoms as indicated in guidelines.^2,42,43 Exemplary quotes in our study revealed that pulmonary and palliative care clinicians recognized that some patients with less severe airflow obstruction may have high symptom burden that could warrant early palliative care. However, some seemed reluctant to refer a patient to early palliative care before progression to more severe stages. Limiting palliative care access to more advanced COPD on spirometry instead of earlier in the disease trajectory based on symptoms misses a clear opportunity to improve quality of life and to have earlier discussions about values and preferences before the end of life.⁴⁴ Furthermore, quality of life is not inextricably linked to lung function by spirometry, and qualitative data reveal that training in successful coping, a hallmark of early palliative care interventions, moderates this experience.^45,46

Our cohort described frequent hospitalizations and emotional symptoms as two priority referral criteria discussed by many clinicians across specialties. The criteria of frequent hospitalizations has been used to identify potential older adults who may qualify as having serious illness and is a strong predictor of mortality in COPD.^47,48 Furthermore, in one study of clinicians caring for COPD patients posthospitalization, using the surprise question (“Would you be surprised if this patient died within 12 months?”) accurately identified COPD patients who may benefit from palliative care and was raised as a potential referral criteria by palliative care clinicians in our cohort.⁴⁹ The second priority referral criterion discussed by many clinicians in our cohort was emotional symptoms. Emotional symptoms negatively impact many outcomes in COPD and are routinely managed as a pillar of early palliative care.^50,51 We have previously demonstrated that emotional symptoms are associated with hospital readmissions, and the presence of clinically elevated emotional symptoms are not just limited to end-stage COPD, where traditional palliative care trials are focused.^50,52 However, without proper training, many pulmonologists do not routinely screen for emotional symptoms, and emotional symptoms are not readily recorded in the electronic medical record. Thus, the use of emotional symptoms as a criterion for referral may be challenging to implement on a wider scale. In a previous analysis, we demonstrated that African Americans, men, and the uninsured have the greatest risk for having unmet mental health care needs in COPD,⁵² which may be useful in guiding risk stratification for emotional symptoms measurement.

As educational opportunities are increasingly available to pulmonologists and consensus referral criteria are established, operational barriers still exist. In our cohort, participants identified several potential operational barriers to integrating early palliative care in COPD. These practical concerns centered around insufficient time to conduct comprehensive palliative care in busy pulmonary clinics, inadequate financial reimbursement for providing palliative care, and limited access to specialist palliative care. These barriers will only be magnified in the setting of a rapidly growing population of older COPD patients outpacing the limited palliative care workforce.⁵³ This is particularly concerning in rural areas where COPD is prevalent, and palliative care access is limited.^54,55 Our cohort raised potential facilitators to address these concerns that included investing in novel models for palliative care delivery such as telehealth palliative care, expanding the workforce of pulmonary nurses trained in palliative care, and embedding palliative care specialists in clinic with pulmonary clinicians. Embedded models of palliative care are feasible and have been shown to improve outcomes for patients with advanced cancer and heart failure, although may not be feasible in rural areas.^56–59 As part of the broader formative evaluation goal of our work, the data from this study informed the development of a nurse-led early palliative care intervention that could address many of the identified barriers and would be feasible across multiple settings. Nurse-led early palliative care models improved quality of life, mood, and survival in advanced cancer.^9,60 These types of palliative care models directly align with the shift to value-based payment and are tangible facilitators on which to focus policy efforts.

Several limitations of this study are acknowledged. Although thematic saturation was achieved, the number of participants in this study is small and limited to clinicians practicing in the southeast. Further research exploring diverse samples of clinicians by race and gender nationwide is warranted. Finally, a survey strategy may have helped to better identify potential referral criteria for early palliative care in COPD, much as Duenk et al. conducted in a cohort of pulmonologists from the Netherlands.¹⁵ However, that study left the objective of defining referral criteria unfulfilled, whereas our in-depth interviews identified priority criteria that could guide future research efforts.

Conclusion

Pulmonary and palliative care clinicians support early palliative care in COPD; however, educational, clinical, and operational barriers hinder implementation. The misconception by pulmonologists that palliative care is tantamount to end-of-life care, the concerns about opioids and benzodiazepines in COPD, and the difficulty in establishing prognostic awareness were significant barriers that could be addressed by broader educational efforts and expanded primary palliative care training in pulmonary medicine. We identified several facilitators, including innovative palliative care delivery models, which could improve early palliative care access in COPD. Finally, we identified several potential priority early palliative care referral criteria that could guide future research. The data from this study have guided the development of a nurse-led early palliative care intervention in COPD.⁵

Footnotes

Funding Information

This research was supported by the Agency for Healthcare Research and Quality, which did not directly contribute to the study.

A.S.I. is supported by a University of Alabama at Birmingham (UAB) Patient Centered Outcomes Research K12 (K12HS023009) from the Agency for Healthcare Research and Quality, a Palliative Research Enhancement Project pilot award from the UAB Center for Palliative and Supportive Care, and other support from the UAB Center for Outcomes and Effectiveness Research and Education. J.N.D.O. is funded by the National Institute of Nursing Research (R00NR015903). C.J.B. is supported in part by a VA Rehabilitation R&D Scientific Merit Award (1I01RX001995). M.T.D. is supported by grants from NIH (1K24HL140108), Department of Defense, American Lung Association, contracted clinical trials from AstraZeneca, Boehringer Ingelheim, GlaxoSmithKline, PneumRx/BTG, Pulmonx, and reports consulting from AstraZeneca, GlaxoSmithKline, Mereo, and PneumRx/BTG. M.A.B. receives support from NR013665-01A1, NR011871-01, PCORI PLC-1609-36381, PLC-1609-36714.

Author Disclosure Statement

D.M.K., L.O.H., and R.O.T. have no conflicts to report.

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