Palliative Care in Advanced Lung Disease: The Challenge of Integrating Palliation Into Everyday Care.

Page 1 of 26

ONLINE FIRST This is an Online First, unedited version of this article. The final, edited version will appear in a numbered issue of CHEST and may contain substantive changes. We encourage readers to check back for the final article. Online First papers are indexed in PubMed and by search engines, but the information, including the final title and author list, may be updated on final publication. http://journal.publications.chestnet.org/

Online First articles are not copyedited prior to posting. ©American College of Chest Physicians. Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details.

Downloaded From: http://journal.publications.chestnet.org/ by a Weill Med College/Cornell University User on 04/27/2015

Page 2 of 26

Palliative Care in Advanced Lung Disease- The Challenge of Integrating Palliation into Everyday Care

1

Graeme Rocker MHSc, DM FRCPC, FRCP, FCCP, A. Catherine Simpson MDiv, PhD 3 Robert Horton MD, CCFP 2

1 Division of Respirology, Medical Director INSPIRED COPD Outreach ProgramTM, Capital Health, Halifax, Nova Scotia, Canada TM

2 INSPIRED COPD Outreach Program , Capital Health, Halifax, Nova Scotia, Canada 3 Division of Palliative Medicine, Capital Health Integrated Palliative Care, Halifax, Nova Scotia, Canada

Address for correspondence: Dr GM Rocker Professor of Medicine Dalhousie University/QEII Health Sciences Centre #4457 Halifax Infirmary 1796 Summer Street Halifax, NS, Canada Word Count 3500 Abstract Word Count 242 References: 75 Key Words: Recent Advances in Chest Medicine, Palliation, Dyspnea, Opioids, INSPIRED COPD Outreach ProgramTM

Conflict of Interest: None of the authors have any conflicts to report

1 Downloaded From: http://journal.publications.chestnet.org/ by a Weill Med College/Cornell University User on 04/27/2015

Page 3 of 26

Abstract The tendency toward 'either/or' thinking (either cure or comfort) in traditional biomedical care paradigms does little to optimize care in advancing chronic illness. Calls for improved palliation in chronic lung disease mandate a review of related care gaps and current clinical practices. While specialist palliative services have their advocates, adding yet another element to an already fragmented, often complex care paradigm will be a challenge. Instead we propose a more holistic, patient-centred approach based on elements fundamental to palliative and best care practices generally and integrated as needed across the entire illness trajectory. To support this approach we review the concept of primary palliative care competencies, identify vulnerability specific to those living with advanced COPD (an exemplar of chronic lung disease), and describe the need for care plans shaped by patient-centred communication, timely palliative responsiveness, and effective advance care planning. A costly systemic issue in the management of chronic lung disease is patients' increasing dependency on episodic emergency room care to deal with preventable episodic crises and refractory dyspnea. We address this issue as part of a proposed model of care that provides pro-active, collaborative case management and the appropriate and carefully monitored use of opioids. We encourage and support a renewed primary care resolve to integrate palliative approaches to care in advanced lung disease that, in concert with judicious referral to appropriate specialist palliative care services, is fundamental to what should be a more sustainable systematic improvement in palliative care delivery.


Page 4 of 26

Introduction At the end of a recent editorial entitled “Science supporting the art of medicine: Improving the management of breathlessness", Sara Booth, one of the UK’s most accomplished palliative care researchers, calls for “renewed confidence in what palliative care has always epitomized”(1). The traditional aims of palliative care are to relieve suffering and improve the quality of life for patients and families who live with advanced illness. This is accomplished through effective and empathetic communication with patients and family members; meticulous attention to addressing pain and other symptoms; psychosocial, spiritual, and bereavement support; and coordination of an array of medical and social services (2). These goals align well with the needs of patients and families living with advanced lung disease and especially those with COPD, and yet are seldom included in the standard approach to their care.

Practice leaders contend that when the need exists, palliative care can and should be a standard offering within regular medical practice (2). Recent Professional Society consensus statements and clinical practice guidelines (3-6) have promoted more holistic, collaborative and integrated approaches to care, including palliation, in the context of advanced chronic lung diseases like COPD. The 2012 American Thoracic Society's (ATS) update on the mechanisms, assessment, and management of dyspnea affirms that dyspnea, the cardinal symptom of lung disease, is responsible for approximately 50% of tertiary care center admissions (5). While the financial costs related to acute care of dyspnea in the US have been estimated at approximately $18 billion (7), the human cost is also huge. Patients in the latter stages of advanced lung disease experience deterioration in symptoms and quality of life on a scope similar to those with advanced malignancy and compared to patients with lung cancer, experience greater escalation of dyspnea and global distress as the illness progresses and functional status deteriorates, but over a longer trajectory (8). These realities warrant significant changes to current models of care (9) and provision of effective palliation if patients and families are to receive the comprehensive care they have requested, need and deserve (10).

Despite the recognized need, efforts to provide effective palliation often fall short for patients and families living with chronic respiratory disease (11). Extensive evidence attests to multiple unmet needs and a lack of access to specialized palliative care that could address them (8, 12). The situation is even worse for patients living and dying with pulmonary fibrosis who have received scant attention until


Page 5 of 26

recently (13-15). This narrative review highlights some areas where particular attention is needed to advance the field of palliation for non-malignant respiratory disease, with COPD as the major focus. The review includes: the types of palliative care services that should be available; the rationale and outline for more effective advance care planning; strategies to reduce reliance on emergency room services; managing dyspnea crises; the safe use of opioids over the longer term and proposed new models of care. Understanding palliative care services There’s a clear distinction to be made between "specialist" palliative care, which provides multidisciplinary expertise plus team-based care within coordinated structured programs, and "primary" palliative care, which aims to integrate palliative approaches within the regular care plan to address unmet needs in the advanced stages of illness. Evidence is beginning to accumulate that beyond metastatic cancer (16, 17) specialized palliative care can lead to improved outcomes(18, 19). Specialist palliative medicine is conceptualized and practiced quite differently in the US than in Canada and the UK. Much of the variation lies in differing opportunities and barriers inherent in socialized vs. free-market health care systems. In Canada and the UK, while national advocacy and professional organizations promote access to specialized palliative care for all patients with advanced illness, in practice, provision of palliative care continues to be rationed by prognosis because an insatiable demand outstrips current resources within a publically funded system. In contrast, in the US, Palliative Medicine, the fastest growing sub-specialty in medicine(19), seeks an expanded role in all chronic illness to complement its traditional association with hospice and end-of-life care. Some within the discipline would further specialize the role of palliative medicine in caring for patients with serious and advanced illness. However, the approach to care on which palliative medicine rests is actually fundamental to good medical care in general (20). Though there is clearly a place for specialized palliative care in more complex cases, a palliative approach to care based on need can and should be rewoven into the fabric of clinical care in all disciplines (20). Arguably, no other illness illustrates this more clearly than COPD, which often exists within a context of complex co-morbidity. Many patients and caregivers living with this illness become increasingly isolated due to progressive breathlessness and debility and have unmet needs arising from poor symptom control, unclear prognosis, inadequate advance care planning and insufficient social and psychological supports (21). An aging population and increasingly complex chronic illness burden factor into the rising demand for specialist palliative care


Page 6 of 26

support, recognizing that these demands cannot yet be adequately addressed by such a specialized model(22). In the case of COPD, a cohesive, patient-centred approach would need to be responsive to needs across the illness trajectory. This would mandate enhanced palliative competencies (22) as well as best practices for primary care and pulmonary medicine (23-25). With appropriate mentorship and linkages this type of team-based approach inclusive of a palliative approach to care can be achieved by disciplines outside of specialized palliative medicine services (26, 27). Providing expert support in the management of complex advanced cases of COPD would continue to be the purview of specialized palliative care along with education and mentorship of colleagues in other disciplines (22, 28). How best to integrate palliative care in the setting of advanced lung disease is more than an academic consideration. Randomized controlled trials of specialized palliative care in COPD are underway (29). To date palliative care provision in this population has yet to be informed by the same quality of evidence that has accrued in the cancer setting. As others have noted, until various models and programs are rigorously implemented and evaluated, the "who, what and how" of palliative care provision in this patient population will remain open to experimentation (20) and the profound vulnerability inherent in unmet needs will persist. Vulnerability and patient-centred care in advanced COPD Many patients and caregivers living with advanced COPD experience significant vulnerability arising from low socioeconomic status and education levels, high co-morbidity, and social isolation. In addition they contend with constraints due to dyspnea, immobility, and oxygen related equipment, and a panoply of emotional, psychological and existential concerns related to loss of meaning/purpose, hope, and fear of death. Social and medical stigma associated with this smoking-related disease, the symptoms of which are often invisible to observers, simply compounds the situation (10, 30-32). This has led one author to characterize these patients as the "disadvantaged dying" (33). Current models of care tend to lack attention to this vulnerability with its attendant psychosocial and spiritual suffering despite professional guidelines(30) and organizational commitments to patient/family-centred care (30, 34, 35). Because this is embedded within a largely unpredictable, progressively downward trajectory, the current 'either/or' thinking (either cure or comfort) of biomedical care paradigms results in costly gaps in care (34-36). A more patient/family centred, "both/and" model would be responsive to evolving patient and caregiver needs--emotional, social, and spiritual as well as physical. Patient-/family-centred care has been defined as ‘‘a partnership among patients, families, and health care providers to design patient-specific education and support to assist in making decisions that are respectful of the patient’s needs and


Page 7 of 26

wishes’’. A more collaborative, patient-centred approach inclusive of palliative care for those living with advanced COPD requires the facilitation of effective communication between patients, caregivers, clinical team members and colleagues. One element of this is clarifying a patient's goals of care through to end of life via a process of effective advance care planning. Advance Care Planning from a patient-centred perspective Patients and caregivers living with advanced COPD are offered few opportunities to discuss goals of care even in final stages despite calls for more effective advance care planning (37, 38) and research to show that many would welcome such discussions(31), that preferences recorded in medical charts are often discordant (39), and that simple strategies can be effective(40) . If these conversations do occur, they often are reduced to a "code status" talk during a severe illness crisis. Frequently this becomes a oneway doctor-to-patient presentation of the 'facts' framed (often unconsciously) to encourage the decision the clinician believes to be best (41). Although this may represent good clinical judgment in terms of an appropriate shift in goals of care, there is often a lack of communication to prepare the patient and caregivers for this shift, its implications, and associated decisions (42). Also caregivers/decision-makers they delegate may not be invited or available to participate in this conversation and thus are not able to advocate on behalf of the patient and his/her care preferences.

In contrast to this last minute, crisis type decision-making, advance care planning (ACP) is a more deliberate, organized, and ongoing process of communication to help an individual identify, reflect upon, discuss, and articulate values, beliefs, goals, and priorities to guide personal care decisions up to and including end-of-life care (43). Elements include a trained facilitator (not necessarily a physician) skilled in relational communication techniques; inclusion of caregiver(s) and/or delegate decisionmaker; attention to patient-related information needs, contextual factors, therapeutic relationship, and illness beliefs and readiness (44, 45). Authentic ACP is about more than filling in a document and/or naming a delegate decision-maker, although it may include either or both of these elements. Evidence suggests that the discussion is equally or more important than any document arising from it (44, 46). What advance care planning might look like in advanced lung disease A skilled ACP facilitator can weave ‘‘care’’ throughout the interaction by eliciting patients’ illness experiences, especially unmet current care needs, seeking to understand their perspectives, exploring


Page 8 of 26

their fears and hopes, identifying and addressing meaningful uncertainties and suffering, engaging hope, and responding to current care needs by the provision of relevant, accessible information, psychosocial/spiritual support and timely referrals as appropriate (see text box). In this way ACP becomes an end in itself (one element in the regular care spectrum) rather than just a means to an end (personal directives or "code status"). Being committed to discovering patients’ hopes and fears and discussing ways to address these is key to creating an individually meaningful framework in which to ground the discussion of goals of care through to the end of life. This should include whether or not use of any technology (e.g.non-invasive ventilation and high flow oxygen delivery systems) fits within these goals (see Appendix 1). Conducting these discussions in patients' homes whenever possible (25) can enhance accessibility, comfort level, and the overall care experience. Wherever these discussions occur we should ensure that as in any medical encounter, there is a necessary skill set that is acquired during medical training through effective mentorship and observation. The final step of sharing ACP insights with other team members involved in the broader supportive approach is necessary to bring about care more concordant with patients’ wishes.

Initiating an ACP discussion

1. Most important first step is to develop or build on an existing therapeutic relationship by: • listening more than talking - what does the patient/carer want to talk about • verbalizing empathy - follow-up on emotion - e.g., "you sound angry about that...?" and then, seek insight into the emotion, where is it coming from, what does it mean (to the patient and/or carer) • seeking clarification or further information about things that are not clear to you • keep in mind that the goal is not a final decision about code status, goals of care, or completing a document, but decisional-readiness • It is about facilitating understanding, reflection, and discussion so that the patient and/or his/her substitute decision-maker is able to make an informed choice as to his/her overall goals of care and care preferences

Reducing Dependence on Episodic and Emergency Room Care


Page 9 of 26

In the latter stages of lung disease, most patients are housebound by increasing frailty and breathlessness and dependent on significant assistance from caregivers. Without adequate planning many lack sufficient and proactive medical follow-up at home once they are no longer able to attend ambulatory primary care visits. Thus they resort to episodic or emergent care through ER presentations in order to manage escalation of symptoms (47). A retrospective analysis of ER utilization in the last months of life for more than 4000 patients over age 65 in the US revealed that more than half visited the ER in the 30 days before death, with 1 in 10 presenting to the ER on the last day of life. More than 40% made multiple visits during their last six months. In contrast, patients who enrolled in hospice programs rarely visited the ER in the last month of life (48). Many with high symptom burden in the latter stages of chronic illness would prefer to avoid the ER. Where care is fragmented, reactive and hampered by diffusion of clinical responsibility across multiple care providers (11, 24, 49) patients have few alternatives. Without access to reliable alternative integrated models of care attuned to their needs (50-53), patients and caregivers remain caught in a repeating cycle of ER presentation, hospital admission and subsequent discharge back to the healthcare system that initially failed them, only to await their next exacerbation or dyspnea crisis.

Dyspnea crisis Dyspnea crisis has been defined as a sustained and severe resting discomfort in patients with advanced—often life-limiting—illness that overwhelms the patient and caregiver’s ability to achieve symptom relief (54). It is one of many factors that lead to intensive utilization of acute care resources in advanced lung disease. Any care plan that aims to reduce this pattern of reliance on reactive and emergent care must have an anticipatory individualized action plan. The ATS document extends previous work in this area by other professional societies (55) by providing some practical strategies and approaches, summarized as the COMFORT approach (Fig 1) (54). Others have focused on the concept of episodic dyspnea, seeking consensus definitions and approaches (56). In any approach, action plans that help patients and families cope with dyspnea crises typically provide a written graduated course of interventions that begins with behavioral and non-pharmacologic interventions such as recovery positions and pursed lip breathing and progress through utilization of inhaled bronchodilators (where there is airflow obstruction) and careful titration of home oxygen (where indicated), and escalate to the use of opioids +/- anxiolytics if intolerable symptoms persist (25).


Page 10 of 26

As symptoms become more advanced and episodic dyspnea crises more prevalent, sublingual fentanyl is a possible option. The research supporting its use for aborting dyspnea crises is sparse as yet and not surprisingly the findings of a recent systematic review were neutral (57). In our experience sublingual fentanyl (starting dose 12.5 – 25ug using 50ug/ml i.v. preparation ) can have positive effects for some patients, (with rapid onset of action due to absorption through mucous membranes) but recipients should be chosen carefully (not for use in opioid naïve patients) and their responses monitored closely. Other commercially available and high dose preparations of fentanyl (designed for pain relief via buccal tablets/sprays) are too potent for dyspnea. The use of fentanyl in palliation has been considered in detail in a recent review(58). Patients and caregivers tend to be more open to/less fearful of using opioids when previous treatment of crisis dyspnea has failed. Video footage of a daughter describing her and her mother's experience with sublingual fentanyl can be found on the Kaiser Permanente website (59). Not unlike the situation where patients have access to a 'help line' via our community outreach program (25), just knowing help is close at hand (via opioids such as fentanyl) can reduce levels of stress.


Page 11 of 26

Attitudes towards longer term use of opioids for dyspnea refractory to conventional treatment The options available to treat refractory dyspnea are well outlined elsewhere (4, 60, 61) and are beyond the scope of this article. Nevertheless there have been some important developments in our understanding of use of opioids (62) which merit further attention. It would be quite understandable for patients and families to have concerns about taking a type of medication typically used for pain, and long associated with death and dying. In contrast, in one study patients who had taken an opioid to relieve dyspnea reported positive experiences, as did their family caregivers (63). This was in stark contrast to opinions expressed by numerous physicians, whose resistance to using opioids for dyspnea was related to legal challenges and professional approbation (63). There were similar findings in a recent UK study(64). To date there have been two long-term observational trials where effects of opioids for refractory dyspnea in COPD have been assessed over months. Both the recent Australian (65) and Canadian (66) trials have extended findings of an earlier systematic review (67) while providing safety data and confirming that carefully initiated, titrated and monitored use of opioids can provide patients with significant relief from dyspnea over a longer term without undue side effects (66). As well, when a 'start low, go slow' approach was used and the patients were asked to rate 10 typical opioid side effects, none were rated worse than symptoms experienced before starting opioids (66) (Table 1). Patients found opioids a helpful adjunct to their conventional treatment and recommended this approach to others (66). More recently a large population study from Sweden suggests that there is no excess mortality when opioids are used in low doses (defined as less than 30 mg oral morphine equivalent per 24 hours) (68). No other medications have yet been proven to be as effective for refractory dyspnea, including benzodiazepines (69). The literature often focuses on success or failure of individual pharmacotherapies in reducing dyspnea intensity. While knowledge, comfort and experience with the pharmacotherapy of refractory dyspnea are all important, we contend that the design and delivery of care has an equally profound impact on patient and caregiver experiences in the latter stages of illness (70). Insert TABLE 1 here Integrating Effective Palliation Within New Models of Care The Patient Centered Medical Home (PCMH) is one promising framework that seeks to transform care of chronic illness from reactive to anticipatory care that encourages the primary care team to work collaboratively with patients and caregivers. The underlying framework promotes system re-design,


Page 12 of 26

optimization of clinical information systems, decision support for clinicians and patient selfmanagement (52, 53). Though no one model can claim superiority in overcoming current deficiencies in care, there is evidence that strategies integrating at least two components of Wagner’s chronic care model are associated with significantly lower hospitalization rates, shorter lengths of stay, and fewer emergency room/unscheduled visits and decreased costs(71). We have reported elsewhere some preliminary findings from the INSPIRED COPD Outreach ProgramTM from Halifax Nova Scotia(25). The latest published data (26) suggests that a multidisciplinary outreach program with a focus on palliation across care transitions can support patients who wish to die at home. A home death from respiratory disease will often exceed the coping capacity of even the most committed family members. The use of complimentary skills of respiratory therapists, palliative medicine and spiritual care practitioners (SCP), enabled some patients to stay home longer before a shorter final admission (for those admitted to hospital) (26). The many appreciative comments about INSPIRED in obituaries and correspondence (Table 2), plus occasional requests for the team SCP to conduct funerals (personal observation) attest to the positive impact of these outcomes. The INSPIRED approach to comprehensive support and practical community and home-based palliation is currently being broadly implemented and evaluated by 19 teams taking part in a new pan-Canadian INSPIRED collaborative (26). Initiatives such as INSPIRED can respond to the many calls for provision of a more ‘both/and’ approach to effective palliation in concert with ongoing medical care for patients who live and die with advanced lung disease. Currently effective care delivery continues to be hindered by deficiencies in continuity, communication and collaboration between health professionals and uncertainties about illness trajectory. Insert Table 2 here Overcoming these deficiencies through a ‘both/and’ approach will require a commitment by professional societies and funders to support and sustain innovative approaches to care (9, 72) that include strategies to ensure effective palliation in advanced lung disease. Engaging patients and families in assessment of respiratory distress (73), working with colleagues to accelerate the pace of uptake of new knowledge(74) and combining evidence based medicine with quality improvement initiatives (26) are examples of a move away from traditional thinking. While successful models of care may differ substantively based on variations in local medical culture, expertise and resource availability, Table 3 proposes key components for successful delivery of palliative care in advanced lung disease.


Page 25 of 26

• Evidence of anxiety or distress over feeling as if life is out of control (or evidence that the patient is a person who likes to be/has been "in control", i.e., the decision-maker in the family, someone who likes things to be black-andwhite, not grey or uncertain) • Particular hopes and/or fears related to progressing COPD - fear of being kept alive indefinitely on a machine, fear of dying without dignity, fear of becoming "a vegetable" (explore what the patient means by terms like dignity, vegetable, peaceful, etc.), hope for a peaceful death or "dying with dignity." 6. Introduce the topic of advance care planning (ACP) • Have you heard the term? What does it mean to you? Have you heard of something called a "living will"? • Build on what they have already told you, e.g., information from the stories, references, or responses to questions about past ED, hospital, family COPD, or death experiences • Acknowledge that many people find the topic difficult or uncomfortable, thinking about getting sicker and dying is not easy and there is a lot of uncertainty. But the truth is any of us can have something unexpected happen to threaten our lives--I could be in a bad car accident on the way home or be hit by a bus, not killed but be unable to speak for myself to tell doctors what I am willing to have them do in the way of treatment and what I would rather avoid. If I have not talked with my family about these things it puts them in a very stressful situation since they will be asked to make these decisions for me. • Frame it in terms of any natural segues you heard (if any), e.g., "You told me you are worried about being a burden to your family. Advance care planning can lessen that burden--it can actually be a gift to your family because in the middle of a health care crisis when you are too sick to speak for yourself and they are asked to make a decision about your care you will have given them some guidance about what to say. This can be a huge relief at a time that can be very stressful for them." • Explain that there are a number of things to talk about including the different types of personal directives, considering who s/he would want as a substitute decision-maker and what that role involves, identifying his/her overall goals of care, and making sure s/he understands what sort of life-sustaining treatment options might be offered in a COPD-related crisis, the likely benefits and burdens of each, and what his/her preferences might be in this regard. Explain that it is a lot to go over and then leave print materials (Personal Directive template, CPR/No CPR patient information brochure, Help with Breathing information brochure, information on feeding tubes, etc.) with them and suggest they (patient and family member(s)) review these before the next visit. Recommend one or more family members, especially whoever is likely to act as delegate/proxy decision-maker be present for the next discussion if patient comfortable with this • Suggest that it is a good idea to write down any questions or concerns as they come up, especially anything they might want to ask their family doctor or respiratory specialist


Page 26 of 26

Visit 2: • Begin by asking about the materials you left with them--how did they find these brochures? Any questions or concerns? Explain that you would like to get into more detail about the topics you mentioned last time. • Who would you want/trust to speak for you in a health care crisis if you were not able to speak for yourself? • Check his/her understanding of COPD - What do you know about COPD? What do you want to know? Can you tell me about possible complications that might happen with your illness? Have you been hospitalized due to your COPD--what happened to cause that? Do you think this could happen again? Has your doctor talked with you about what might happen? Is this something you have wondered about or are worried about at all? • Quality of Life - what makes life worthwhile for you? What do you enjoy? What would have to be missing for you to feel life was no longer worth living? What makes you want to keep going even when you have a really bad day with your breathing, mobility? • How do you make important decisions - on your own, together with your spouse or family, with help from others who know more about the situation, e.g., your doctor • What you are hoping for (what would a good death look like for you?) • Preferred location of death, who should be present, any religious or spiritual practices • Offer to help patient complete a personal directive if s/he so wishes. Important to emphasize: • Even if patient does not want to do an instructional directive, completing a delegate directive is still a big help to family and healthcare team • A directive is never invoked if the patient is able to speak for him/herself and has capacity • Can be changed any time, as often as the patient wants– just remind them to destroy old copies and redistribute to everyone who got a copy the first time


Page 15 of 26

15. Lindell KO, Liang Z, Hoffman LA, Rosenzweig MQ, Saul MI, Pilewski JM, et al. Palliative Care and Location of Death in Decedents with Idiopathic Pulmonary Fibrosis. Chest. 2014 Sep 4. PubMed PMID: 25187973. 16. Temel JS, Greer JA, Muzikansky A, Gallagher ER, Admane S, Jackson VA, et al. Early palliative care for patients with metastatic non-small-cell lung cancer. The New England journal of medicine. 2010 Aug 19;363(8):733-42. PubMed PMID: 20818875. 17. Zimmermann C, Swami N, Krzyzanowska M, Hannon B, Leighl N, Oza A, et al. Early palliative care for patients with advanced cancer: a cluster-randomised controlled trial. Lancet. 2014 Feb 18. PubMed PMID: 24559581. 18. Higginson IJ, Bausewein C, Relly CC, Gao W, Geysels M, Dzingina M, et al. An integrated and palliative respiratory care service for patients with advanced disease and refractory breathlessness: a randomized controlled trial. Lancet Respir Med. 2014. Epub 2014, Oct 29th. 19. Hughes MT, Smith TJ. The growth of palliative care in the United States. Annual review of public health. 2014;35:459-75. PubMed PMID: 24641562. 20. Johnson M, Fallon M. Just good care? The palliative care of those with non-malignant disease. Palliative medicine. 2013 Oct;27(9):803-4. PubMed PMID: 24058003. 21. Pinnock H, Kendall M, Murray SA, Worth A, Levack P, Porter M, et al. Living and dying with severe chronic obstructive pulmonary disease: multi-perspective longitudinal qualitative study. Bmj. 2011;342:d142. PubMed PMID: 21262897. Epub 2011/01/26. eng. 22. Quill TE, Abernethy AP. Generalist plus specialist palliative care--creating a more sustainable model. The New England journal of medicine. 2013 Mar 28;368(13):1173-5. PubMed PMID: 23465068. 23. Cawley D, Billings J, Oliver D, Kendall M, Pinnock H. Potential triggers for the holistic assessment of people with severe chronic obstructive pulmonary disease: analysis of multiperspective, serial qualitative interviews. BMJ supportive & palliative care. 2014 Mar 28. PubMed PMID: 24681560. 24. Horton R, Rocker G, Dale A, Young J, Hernandez P, Sinuff T. Implementing a Palliative Care Trial in Advanced COPD: A Feasibility Assessment (The COPD IMPACT Study). Journal of palliative medicine. 2013 Jan;16(1):67-73. PubMed PMID: 23317322. Epub 2013/01/16. eng. 25. Rocker GM, Cook D. 'INSPIRED' Approaches to Better Care for Patients with Advanced COPD. Clinical and investigative medicine Medecine clinique et experimentale. 2013;36(3):E114. PubMed PMID: 23739664. 26. Rocker GM, Verma JY. 'INSPIRED' COPD Outreach Program™: Doing the Right Things Right. Clinical and investigative medicine Medecine clinique et experimentale. 2014;37(5):E311. PubMed PMID: 25282137. 27. Kendall M, Buckingham S, Ferguson S, Sheikh A, Murray S, Macnee W ea. Helping people with very severe copd: feasibility study of a novel holistic intervention. BMJ supportive & palliative care. 2014;4 (Suppl 1:A9). 28. von Gunten CF. Who should palliative medicine be asked to see? Journal of palliative medicine. 2011 Jan;14(1):2-3. PubMed PMID: 21244246. Epub 2011/01/20. eng. 29. Duenk RG, Heijdra Y, Verhagen SC, Dekhuijzen RP, Vissers KC, Engels Y. PROLONG: a cluster controlled trial to examine identification of patients with COPD with poor prognosis and implementation of proactive palliative care. BMC pulmonary medicine. 2014;14(1):54. PubMed PMID: 24690101. Pubmed Central PMCID: 3995742. 30. Goodridge D, Marciniuk DD, Brooks D, van Dam A, Hutchinson S, Bailey P, et al. End-of-life care for persons with advanced chronic obstructive pulmonary disease: Report of a national interdisciplinary consensus meeting. Canadian respiratory journal : journal of the Canadian Thoracic Society. 2009 SepOct;16(5):e51-3. PubMed PMID: 19851529. 31. Reinke LF, Slatore CG, Uman J, Udris EM, Moss BR, Engelberg RA, et al. Patient-clinician communication about end-of-life care topics: is anyone talking to patients with chronic obstructive


Page 16 of 26

pulmonary disease? Journal of palliative medicine. 2011 Aug;14(8):923-8. PubMed PMID: 21631367. Epub 2011/06/03. eng. 32. Simpson AC, Young J, Donahue M, Rocker G. A day at a time: caregiving on the edge in advanced COPD. Int J Chron Obstruct Pulmon Dis. 2010;5:141-51. PubMed PMID: 20631814. Epub 2010/07/16. eng. 33. Exley C, Field D, Jones L, Stokes T. Palliative care in the community for cancer and end-stage cardiorespiratory disease: the views of patients, lay-carers and health care professionals. Palliat Med. 2005 Jan;19(1):76-83. PubMed PMID: 15690872. 34. Rocker GM, Young J, Simpson AC. Advanced chronic obstructive lung disease: more than a lung disease. Prog Palliat Care. 2009;17:117-25. 35. Simpson AC, Rocker GM. Advanced chronic obstructive pulmonary disease: impact on informal caregivers. J Palliat Care. 2008 Spring;24(1):49-54. PubMed PMID: 18459597. 36. Rocker GM, Sinuff T, Horton R, Hernandez P. Advanced Chronic Obstructive Pulmonary Disease: Innovative Approaches to Palliation. Journal of palliative medicine. 2007;10(3):783-97. 37. You JJ, Fowler RA, Heyland DK. Just ask: discussing goals of care with patients in hospital with serious illness. CMAJ. Apr 1;186(6):425-32. PubMed PMID: 23857860. Epub 2013/07/17. eng. 38. Janssen DJ, Spruit MA, Schols JM, Wouters EF. A call for high-quality advance care planning in outpatients with severe COPD or chronic heart failure. Chest. May;139(5):1081-8. PubMed PMID: 20829337. Epub 2010/09/11. eng. 39. Heyland DK, Barwich D, Pichora D, Dodek P, Lamontagne F, You JJ, et al. Failure to engage hospitalized elderly patients and their families in advance care planning. JAMA Intern Med. 2013 May 13;173(9):778-87. PubMed PMID: 23545563. 40. Au DH, Udris EM, Engelberg RA, Diehr PH, Bryson CL, Reinke LF, et al. A randomized trial to improve communication about end-of-life care among patients with COPD. Chest. 2012 Mar;141(3):72635. PubMed PMID: 21940765. Epub 2011/09/24. eng. 41. Epstein RM, Peters E. Beyond information: exploring patients' preferences. JAMA : the journal of the American Medical Association. 2009 Jul 8;302(2):195-7. PubMed PMID: 19584351. 42. Curtis JR, Engelberg RA, Wenrich MD, Shannon SE, Treece PD, Rubenfeld GD. Missed opportunities during family conferences about end-of-life care in the intensive care unit. Am J Respir Crit Care Med. 2005 Apr 15;171(8):844-9. PubMed PMID: 15640361. 43. Simpson C. Advance care planning in COPD: care versus "code status". Chronic respiratory disease. 2012 Aug;9(3):193-204. PubMed PMID: 22729389. 44. Sudore RL, Fried TR. Redefining the "planning" in advance care planning: preparing for end-oflife decision making. Annals of internal medicine. 2010 Aug 17;153(4):256-61. PubMed PMID: 20713793. Epub 2010/08/18. eng. 45. Sudore RL, Schickedanz AD, Landefeld CS, Williams BA, Lindquist K, Pantilat SZ, et al. Engagement in multiple steps of the advance care planning process: a descriptive study of diverse older adults. Journal of the American Geriatrics Society. 2008 Jun;56(6):1006-13. PubMed PMID: 18410324. 46. Fried TR, Bullock K, Iannone L, O'Leary JR. Understanding advance care planning as a process of health behavior change. Journal of the American Geriatrics Society. 2009 Sep;57(9):1547-55. PubMed PMID: 19682120. Pubmed Central PMCID: 2783892. 47. Horton R. Reducing emergency room utilization in end-stage COPD - feasible or fantasy? Chronic respiratory disease.10(1):49-54. PubMed PMID: 23355405. Epub 2013/01/29. eng. 48. Smith AK, McCarthy E, Weber E, Cenzer IS, Boscardin J, Fisher J, et al. Half of older Americans seen in emergency department in last month of life; most admitted to hospital, and many die there. Health Aff (Millwood). 2012 Jun;31(6):1277-85. PubMed PMID: 22665840. Epub 2012/06/06. eng.


Page 17 of 26

49. Crawford GB, Brooksbank MA, Brown M, Burgess TA, Young M. The unmet needs of people with end-stage chronic obstructive pulmonary disease: recommendations for change in Australia. Intern Med J. 2012 Apr 4. PubMed PMID: 22471972. Epub 2012/04/05. Eng. 50. Simpson AC, Rocker GM. Advanced chronic obstructive pulmonary disease: rethinking models of care. Qjm. 2008 Sep;101(9):697-704. PubMed PMID: 18669555. 51. Booth S, Bausewein C, Rocker G. New models of care for advanced lung disease. Progress in Palliative Care. 2011 //;19(5):254-63. 52. Fromer L. Implementing chronic care for COPD: planned visits, care coordination, and patient empowerment for improved outcomes. Int J Chron Obstruct Pulmon Dis. 2011;6:605-14. PubMed PMID: 22162647. Epub 2011/12/14. eng. 53. Ortiz G, Fromer L. Patient-Centered Medical Home in chronic obstructive pulmonary disease. J Multidiscip Healthc. 2011;4:357-65. PubMed PMID: 22096340. Epub 2011/11/19. eng. 54. Mularski RA, Reinke LF, Carrieri-Kohlman V, Fischer MD, Campbell ML, Rocker G, et al. An official american thoracic society workshop report: assessment and palliative management of dyspnea crisis. Ann Am Thorac Soc. Oct;10(5):S98-S106. PubMed PMID: 24161068. Epub 2013/10/29. eng. 55. Mahler DA, Selecky PA, Harrod CG, Benditt JO, Carrieri-Kohlman V, Curtis JR, et al. American College of Chest Physicians consensus statement on the management of dyspnea in patients with advanced lung or heart disease. Chest. 2010 Mar;137(3):674-91. PubMed PMID: 20202949. Epub 2010/03/06. eng. 56. Simon ST, Weingartner V, Higginson IJ, Voltz R, Bausewein C. Definition, categorization, and terminology of episodic breathlessness: consensus by an international Delphi survey. J Pain Symptom Manage. 2014 May;47(5):828-38. PubMed PMID: 24095285. 57. Simon ST, Koskeroglu P, Gaertner J, Voltz R. Fentanyl for the relief of refractory breathlessness: a systematic review. J Pain Symptom Manage. Dec;46(6):874-86. PubMed PMID: 23742735. Epub 2013/06/08. eng. 58. Stanley TH. The Fentanyl Story. The journal of pain : official journal of the American Pain Society. 2014 Nov 1;15(12):1215-26. PubMed PMID: 25441689. 59. http://share.kaiserpermanente.org/article/helping-patients-with-advanced-disease-breatheeasier-expert-panel-issues-recommendations-for-dyspnea-crisis/ 60. Johnson MJ, Abernethy AP, Currow DC. Gaps in the evidence base of opioids for refractory breathlessness. A future work plan? J Pain Symptom Manage. 2012 Mar;43(3):614-24. PubMed PMID: 22285285. Epub 2012/01/31. eng. 61. Horton R, Rocker G. Contemporary issues in refractory dyspnoea in advanced chronic obstructive pulmonary disease. Curr Opin Support Palliat Care. 2010 Jun;4(2):56-62. PubMed PMID: 20407378. Epub 2010/04/22. eng. 62. Hallenbeck J. Pathophysiologies of Dyspnea Explained: Why Might Opioids Relieve Dyspnea and not Hasten Death. Journal of palliative medicine. 2012;15(8):DOI: 10.1089/jpm.2011.0167. 63. Rocker G, Young J, Donahue M, Farquhar M, Simpson C. Perspectives of patients, family caregivers and physicians about the use of opioids for refractory dyspnea in advanced chronic obstructive pulmonary disease. CMAJ. 2012 Jun 12;184(9):E497-504. PubMed PMID: 22529167. Epub 2012/04/25. eng. 64. Hadjiphilippou S, Odogwu SE, Dand P. Doctors' attitudes towards prescribing opioids for refractory dyspnoea: a single-centred study. BMJ supportive & palliative care. 2014 Mar 6. PubMed PMID: 24644207. 65. Currow DC, McDonald C, Oaten S, Kenny B, Allcroft P, Frith P, et al. Once-daily opioids for chronic dyspnea: a dose increment and pharmacovigilance study. J Pain Symptom Manage. 2011 Sep;42(3):388-99. PubMed PMID: 21458217. Epub 2011/04/05. eng.


Page 18 of 26

66. Rocker GM, Simpson AC, Joanne Young B, Horton R, Sinuff T, Demmons J, et al. Opioid therapy for refractory dyspnea in patients with advanced chronic obstructive pulmonary disease: patients' experiences and outcomes. Canadian Medical Association Open Access Journal. 2013 January 16, 2013;1(1):E27-E36. 67. Jennings AL, Davies AN, Higgins JP, Gibbs JS, Broadley KE. A systematic review of the use of opioids in the management of dyspnoea. Thorax. 2002 Nov;57(11):939-44. PubMed PMID: 116. 68. Ekstrom MP, Bornefalk-Hermansson A, Abernethy AP, Currow DC. Safety of benzodiazepines and opioids in very severe respiratory disease: national prospective study. Bmj.348:g445. PubMed PMID: 24482539. Epub 2014/02/01. eng. 69. Simon ST, Higginson IJ, Booth S, Harding R, Bausewein C. Benzodiazepines for the relief of breathlessness in advanced malignant and non-malignant diseases in adults. The Cochrane database of systematic reviews. (1):CD007354. PubMed PMID: 20091630. Epub 2010/01/22. eng. 70. Booth S, Moffat C, Burkin J, Galbraith S, Bausewein C. Nonpharmacological interventions for breathlessness. Curr Opin Support Palliat Care. 2011 Jun;5(2):77-86. PubMed PMID: 21532347. 71. Adams SG, Smith PK, Allan PF, Anzueto A, Pugh JA, Cornell JE. Systematic review of the chronic care model in chronic obstructive pulmonary disease prevention and management. Arch Intern Med. 2007 Mar 26;167(6):551-61. PubMed PMID: 17389286. Epub 2007/03/29. eng. 72. Booth S, Moffat C, Farquhar M, Higginson IJ, Burkin J. Developing a breathlessness intervention service for patients with palliative and supportive care needs, irrespective of diagnosis. J Palliat Care. 2011 Spring;27(1):28-36. PubMed PMID: 21510129. Epub 2011/04/23. eng. 73. Campbell ML, Templin TN. RDOS-Family: A Guided Learning Tool for Layperson Assessment of Respiratory Distress. Journal of palliative medicine. 2014 Sep;17(9):982-3. PubMed PMID: 25115233. 74. Abernethy AP, Kamal AH, Wheeler JL, Cox C. Management of dyspnea within a rapid learning healthcare model. Curr Opin Support Palliat Care. Jun;5(2):101-10. PubMed PMID: 21455072. Epub 2011/04/02. eng. 75. Murray SA, Firth A, Schneider N, Van den Eynden B, Gomez-Batiste X, Brogaard T, et al. Promoting palliative care in the community: Production of the primary palliative care toolkit by the European Association of Palliative Care Taskforce in primary palliative care. Palliat Med. 2014 Nov 13. PubMed PMID: 25395577.


Page 19 of 26

Figure 1 The COMFORT approach (reproduced with permission from the American Thoracic Society (54)

Legend: The COMFORT approach is a “customizable caregiver plan for episodes of crisis dyspnea” (54) that can be completed ahead of time following discussion between physician and family member.


Page 20 of 26

Table 1. A comparison of two recent observational trials of long term use of opioids for refractory dyspnea related to COPD

Patients enrolled Median age Primary diagnosis of COPD Baseline dyspnea severityModified Medical Research Council (MMRC) Baseline dyspnea intensity (mean) Patient experience recorded/described

Starting/maintenance regime

Rocker et al 2013 (66)

Currow et al 2011 (65)

45 74 100%

83 76.5 54%

MMRC 3 – 18% MMRC 4 – 82%

MMRC 3 – 25% MMRC 4 – 75%

7/10 NRS

50.3/100 VAS

Yes

No

Morphine IR 0.5 mg BID, increasing to 1mg QID by 7 days and further weekly increases according to patient scores of tolerability of dyspnea

Morphine SR 10mg OD, increasing weekly to 20mg or 30 mg OD if lower dose ineffective

Mean daily opioid dose at end trial (oral morphine equivalent) Duration of trial % enrolled patients finding opioids beneficial at end of trial

10.2 mg

14.0 mg

4 – 6 months

3 months

61%

33%

Side Effects

10 typical side effects scored by patients, none worse than at baseline

13 withdrawals due to side effects of constipation (n=6), drowsiness (n=4), nausea/vomiting (n=4)

Statistically significant outcomes versus baseline HRQoL

Median (IQR)

Mean

∆ CRQ: 0.6 (0.1-1.3)

n/a

Dyspnea

∆ CRQ-D: 1.0 (0-1.4)

McGill (symptom ranking)

∆ NRS: -2.0 (-3.0 – 0.0)

-10.7/100 mm (VAS)

Yes, none attributable to opioids

No episodes of respiratory failure or deaths reported

Details of deaths and hospital admissions provided

IR: Immediate release SR: Sustained release HRQoL: Health related quality of Life

CRQ: Chronic Respiratory Questionnaire CRQ- D: CRQ Dyspnea domain NRS: Numerical rating scale VAS: Visual analogue Score


Page 21 of 26

Table 2. How INSPIRED helps: Top Five Patient-reported reasons with illustrative quotes postINSPIRED(26) 1. Action plan and prescriptions on-hand or on-order 2. Accessible education, information and resources 3. Improved outcomes relevant to patient and family, for example, less breathlessness, more stamina, recognition and management of COPD, use of medications 4. Someone to call for guidance and support; and not feeling so alone and abandoned 5. Feeling cared for by caring, reliable, knowledgeable staff using effective communication

“I used to feel so alone with my illness. Now people check on me and I know there’s someone I can call if I’m having a problem. I would feel so isolated, frustrated and apprehensive without this support.” INSPIRED patient “There were times when panic was setting in... It was a tremendous relief to know that I wasn't alone and that there was someone who cared that I could turn to... You handled Mum with such dignity and respect that I can never thank you enough!” INSPIRED family caregiver “She was in the ER three times this year, it could have been 12.” INSPIRED family caregiver reflecting on his wife’s final months.


Page 22 of 26

Table 3. Key requirements for successful integration of palliative care in advanced lung disease.

Key Components of Integrated Palliative Care in Advanced Lung Disease • • • • • • • • • • •

Dedicated case manager skilled in medical/psychosocial assessment and collaborative case management across care settings Skilled advance care planning Ongoing home-based follow-up with access to physician assessments when required 24/7 access to after-hours medical support/advice Individualized action plans for managing dyspnea crisis and AECOPD In-home support and education from a skilled COPD educator/respiratory therapist Direct hospital admission that bypasses the ER where indicated Affordable and reliable home support and personal care Accessible respite care for family caregivers Seamless linkage to in-home hospice care for those nearing end-of-life Team access to responsive specialist Respirology and Palliative Medicine expertise


Page 24 of 26

Appendix 1 Conducting an ACP discussion

It is best to spread the initial discussion over several visits Visit 1 1. Ask about and listen to the illness experience, e.g., What has it been like living with COPD? How has life changed? What do you miss most? What has been hardest for you? What has helped you cope, e.g., Thinking about hard times in the past, what helped you get through these? Is this what is helping you deal with COPD now? Do you have any cultural, religious, or spiritual beliefs that are important to you or help you manage? Listen for any references to or stories (or ask) about: • previous ED or hospital experiences; family members or friends with COPD What was this like? Did it make you think any differently about your own situation? • death of family member or friend What was this like? Was it a “good” death in your view--why or why not? 2. Ask about the patient's hopes - what are you hoping for? What would you like to have happen? In a perfect world? Given that there is not yet any cure for this illness...is there anything you are especially looking forward to? 3. Ask about the patient's fears, worries, concerns. Are you worried at all about your COPD, how it is affecting you, your life, your family (e.g., being a burden)? Have you thought at all about dying--are you wondering/worried about what it might be like (e.g., suffocation, gasping for breath, unrelieved suffering)? Is there anything you think might happen or have been told or seen that you are concerned about (e.g., being kept alive on a machine; becoming a vegetable; being euthanized)? 4. Explore what "living well" means to the patient - From what you have told me your COPD has changed your life, but your life is still worth living. What do you think makes it that way even though you are not able to do all the things you used to enjoy? What do you need to have in order for you to enjoy your life or live well? i. What gives life meaning for you? ii. What makes life worth living? What keeps you going? iii. What would have to be missing for you to feel like life was no longer worth living? 5. Through all of this listen for/identify spontaneous ACP segues provided by patient, e.g. • Fear of being a burden to loved ones


Page 25 of 26

• Evidence of anxiety or distress over feeling as if life is out of control (or evidence that the patient is a person who likes to be/has been "in control", i.e., the decision-maker in the family, someone who likes things to be black-andwhite, not grey or uncertain) • Particular hopes and/or fears related to progressing COPD - fear of being kept alive indefinitely on a machine, fear of dying without dignity, fear of becoming "a vegetable" (explore what the patient means by terms like dignity, vegetable, peaceful, etc.), hope for a peaceful death or "dying with dignity." 6. Introduce the topic of advance care planning (ACP) • Have you heard the term? What does it mean to you? Have you heard of something called a "living will"? • Build on what they have already told you, e.g., information from the stories, references, or responses to questions about past ED, hospital, family COPD, or death experiences • Acknowledge that many people find the topic difficult or uncomfortable, thinking about getting sicker and dying is not easy and there is a lot of uncertainty. But the truth is any of us can have something unexpected happen to threaten our lives--I could be in a bad car accident on the way home or be hit by a bus, not killed but be unable to speak for myself to tell doctors what I am willing to have them do in the way of treatment and what I would rather avoid. If I have not talked with my family about these things it puts them in a very stressful situation since they will be asked to make these decisions for me. • Frame it in terms of any natural segues you heard (if any), e.g., "You told me you are worried about being a burden to your family. Advance care planning can lessen that burden--it can actually be a gift to your family because in the middle of a health care crisis when you are too sick to speak for yourself and they are asked to make a decision about your care you will have given them some guidance about what to say. This can be a huge relief at a time that can be very stressful for them." • Explain that there are a number of things to talk about including the different types of personal directives, considering who s/he would want as a substitute decision-maker and what that role involves, identifying his/her overall goals of care, and making sure s/he understands what sort of life-sustaining treatment options might be offered in a COPD-related crisis, the likely benefits and burdens of each, and what his/her preferences might be in this regard. Explain that it is a lot to go over and then leave print materials (Personal Directive template, CPR/No CPR patient information brochure, Help with Breathing information brochure, information on feeding tubes, etc.) with them and suggest they (patient and family member(s)) review these before the next visit. Recommend one or more family members, especially whoever is likely to act as delegate/proxy decision-maker be present for the next discussion if patient comfortable with this • Suggest that it is a good idea to write down any questions or concerns as they come up, especially anything they might want to ask their family doctor or respiratory specialist


Page 26 of 26

Visit 2: • Begin by asking about the materials you left with them--how did they find these brochures? Any questions or concerns? Explain that you would like to get into more detail about the topics you mentioned last time. • Who would you want/trust to speak for you in a health care crisis if you were not able to speak for yourself? • Check his/her understanding of COPD - What do you know about COPD? What do you want to know? Can you tell me about possible complications that might happen with your illness? Have you been hospitalized due to your COPD--what happened to cause that? Do you think this could happen again? Has your doctor talked with you about what might happen? Is this something you have wondered about or are worried about at all? • Quality of Life - what makes life worthwhile for you? What do you enjoy? What would have to be missing for you to feel life was no longer worth living? What makes you want to keep going even when you have a really bad day with your breathing, mobility? • How do you make important decisions - on your own, together with your spouse or family, with help from others who know more about the situation, e.g., your doctor • What you are hoping for (what would a good death look like for you?) • Preferred location of death, who should be present, any religious or spiritual practices • Offer to help patient complete a personal directive if s/he so wishes. Important to emphasize: • Even if patient does not want to do an instructional directive, completing a delegate directive is still a big help to family and healthcare team • A directive is never invoked if the patient is able to speak for him/herself and has capacity • Can be changed any time, as often as the patient wants– just remind them to destroy old copies and redistribute to everyone who got a copy the first time


Integrating palliative care into the trajectory of cancer care.

Integrating palliative care into active cancer treatment.

Integrating Palliative Care into Critical Care: A Quality Improvement Study.

Primary palliative care for the general internist: integrating goals of care discussions into the outpatient setting.

Integrating palliative care in the ICU.

Integrating palliative and cancer care.

Palliative care of chronic progressive lung disease.

Palliative care of chronic progressive lung disease.

Palliative care of chronic progressive lung disease.

Palliative care in Africa: a global challenge.

Kenya Hospices and Palliative Care Association: integrating palliative care in public hospitals in Kenya.

Integrating PoCT into Clinical Care.

Integrating acupuncture into cancer care.

Integrating palliative care in the nursing home: an interprofessional opportunity.

Integrating HIV and palliative care: ending the false dichotomy.

Integrating palliative care into national health systems in Africa: a multi-country intervention study.

Integrating Palliative Care Into Comprehensive Cancer Centers: Consensus-Based Development of Best Practice Recommendations.

Integrating palliative care into self-management of breast cancer: Protocol for a pilot randomized controlled trial.

ESMO Clinical Practice Guidelines on palliative care: advanced care planning.

Integrating palliative care in oncologic emergency departments: Challenges and opportunities.

Inadequate Palliative Care in Chronic Lung Disease. An Issue of Health Care Inequality.

Palliative care for lung disease: start early, stay late.

Palliative care for advanced practice nurses.

Palliative care in patients with lung cancer.