Review Article

Open Access

Improving patient and caregiver outcomes in oncology: Team-based, timely, and targeted palliative care

Corresponding Author

David Hui , MD, MSc

Associate Professor and Attending Physician

[email protected]

Department of Palliative Care, Rehabilitation, and Integrative Medicine and Department of General Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX

Corresponding author: David Hui, MD, MSc, Department of Palliative Care, Rehabilitation, and Integrative Medicine, Unit 1414, The University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd, Houston, TX, 77030; [email protected]

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Breffni L. Hannon MBChB,

Breffni L. Hannon MBChB

Assistant Professor and Attending Physician

Department of Supportive Care, Princess Margaret Cancer Center, University Health Network, University of Toronto, Toronto, ON, Canada

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Camilla Zimmermann MD, PhD,

Camilla Zimmermann MD, PhD

Professor and Chair

Department of Supportive Care, Princess Margaret Cancer Center, University Health Network, University of Toronto, Toronto, ON, Canada

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Eduardo Bruera MD, FAAHPM,

Eduardo Bruera MD, FAAHPM

Professor and Chair

Department of Palliative Care, Rehabilitation, and Integrative Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX

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David Hui , MD, MSc,

Corresponding Author

David Hui , MD, MSc

Associate Professor and Attending Physician

[email protected]

Department of Palliative Care, Rehabilitation, and Integrative Medicine and Department of General Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX

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Breffni L. Hannon MBChB,

Breffni L. Hannon MBChB

Assistant Professor and Attending Physician

Department of Supportive Care, Princess Margaret Cancer Center, University Health Network, University of Toronto, Toronto, ON, Canada

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Camilla Zimmermann MD, PhD,

Camilla Zimmermann MD, PhD

Professor and Chair

Department of Supportive Care, Princess Margaret Cancer Center, University Health Network, University of Toronto, Toronto, ON, Canada

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Eduardo Bruera MD, FAAHPM,

Eduardo Bruera MD, FAAHPM

Professor and Chair

Department of Palliative Care, Rehabilitation, and Integrative Medicine, The University of Texas MD Anderson Cancer Center, Houston, TX

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First published: 13 September 2018

https://doi.org/10.3322/caac.21490

Citations: 265

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Abstract

Over the past decade, a large body of evidence has accumulated supporting the integration of palliative care into oncology practice for patients with advanced cancer. The question is no longer whether palliative care should be offered, but what is the optimal model of delivery, when is the ideal time to refer, who is in greatest need of a referral, and how much palliative care should oncologists themselves be providing. These questions are particularly relevant given the scarcity of palliative care resources internationally. In this state-of-the-science review directed at the practicing cancer clinician, the authors first discuss the contemporary literature examining the impact of specialist palliative care on various health outcomes. Then, conceptual models are provided to support team-based, timely, and targeted palliative care. Team-based palliative care allows the interdisciplinary members to address comprehensively the multidimensional care needs of patients and their caregivers. Timely palliative care, at its best, is preventive care to minimize crises at the end of life. Targeted palliative care involves identifying the patients most likely to benefit from specialist palliative care interventions, akin to the concept of targeted cancer therapies. Finally, the strengths and weaknesses of innovative care models, such as outpatient clinics, embedded clinics, nurse-led palliative care, primary palliative care provided by oncology teams, and automatic referral, are summarized. Moving forward, more research is needed to determine how different health systems can best personalize palliative care to provide the right level of intervention, for the right patient, in the right setting, at the right time. CA Cancer J Clin. 2018;680:00-00. 2018 American Cancer Society, Inc.

Introduction

Despite major advances in cancer therapeutics over the past decades, patients with cancer continue to experience significant morbidity and mortality.1 Cross-sectional studies have reported consistently that patients with cancer experience a median of 8 to 12 symptoms, many of which are underdiagnosed and undertreated.2, 3 In addition to their physical symptom burden, these patients often have other unmet supportive care needs, such as psychological distress, and a need for health information and care planning.4 This supportive care need is further amplified by the finding that the incidence of cancer is increasing worldwide with an aging population and that many patients with advanced cancer are living longer with an incurable illness because of more effective cancer treatments.5

Traditionally, oncologists have played a central role in the delivery of supportive care. Many oncologists see supportive care as an essential component of oncology care and derive satisfaction from providing it.6, 7 Working on the front lines of cancer care, oncologists are invariably involved in palliating cancer-related symptoms, managing treatment side-effects, discussing prognosis, facilitating end-of-life discussions, and referring patients to other specialties.8 However, there is significant variation in the provision of supportive care and palliative care referral among oncologists.9, 10 The increasingly complex oncology therapeutic landscape, coupled with busier clinics, means that it is more and more challenging for the oncology team alone to address supportive care needs comprehensively.8, 11 Meanwhile, the implementation of routine symptom distress screening is uncovering even more supportive care needs among patients with cancer.11, 12 In addition, supportive care itself is becoming increasingly specialized, with a rapidly growing body of knowledge and research.13

Palliative care has evolved over the last few decades from a philosophy of care for dying patients to a professional discipline with expertise in symptom management, psychosocial and spiritual care, caregiver support, patient-clinician communication, complex decision making, and end-of-life care.14, 15 It is particularly well positioned to work alongside oncology teams to address the complex supportive care needs of patients with cancer and their families.16, 17 Importantly, the provision of palliative care should not be limited to the last days or weeks of life, because many of the key domains of care described above can (and should) be provided much earlier in the disease trajectory to improve patient and caregiver outcomes.18

Recognizing the added value of palliative care, many national and international organizations, such as the World Health Organization, the American Society of Clinical Oncology, the American Cancer Society, and the Institute of Medicine, all promote early palliative care involvement alongside standard oncology care.19-22 The relevant question is no longer whether palliative care should be offered, but what is the optimal model of delivery, when is the ideal time to refer, who is in greatest need of a referral, and how much palliative care should oncologists be providing, particularly given the scarcity of palliative care resources internationally. In this state-of-the-science review directed at the practicing oncology clinician, we: 1) discuss the contemporary literature examining the impact of palliative care on care outcomes; 2) provide conceptual frameworks on interdisciplinary, timely, and targeted palliative care; and 3) summarize the strengths and weaknesses of innovative care models, such as outpatient clinics, embedded clinics, nurse-led palliative care, primary palliative care provided by oncology teams, and automatic referral.

Summary/Key Points

The growing number of patients living longer with advanced cancer, coupled with heightened awareness of distress through routine symptom screening, translates into an increasing demand for supportive care.
Palliative care is a professional discipline that is well positioned to work together with the oncology team to support the physical, emotional, social, spiritual, informational, and decision-making needs of patients with cancer and their families throughout the disease trajectory.

Evidence to Support Early Palliative Care

Randomized Controlled Trials

Over the past decade, there has been an explosion of clinical trials comparing concurrent oncologic and palliative care versus usual oncologic care alone in outpatient and inpatient settings, providing level I evidence to support the integration of palliative care along the disease trajectory.23-40 In this section, we focus on more recent publications, because older studies have been summarized in previous reviews.18, 41-43 Table 1 highlights the key elements of study design and outcomes.23-40, 44 A majority of these clinical trials concluded that concurrent palliative care improves quality of life, symptoms, and patient-clinician communication compared with oncologic care alone.25, 26, 29, 31, 37, 39, 44 Some studies also demonstrated that palliative care enhances mood, patient satisfaction, quality of end-of-life care, survival, and caregiver outcomes (Table 1).23-40, 44 Of note, none of the studies favored oncologic care alone for the primary outcome.

Table 1. Randomized Clinical Trials Published Since 2009 Comparing Palliative Care and Usual Oncologic Care Versus Usual Care Alone^a

STUDY	WHO (ADVANCED)	WHEN	WHERE	WHAT	QUALITY OF LIFE	SYMPTOMS	MOOD	SATISFACTION	COMMUNICATION	EOL CARE	SURVIVAL	CAREGIVERS
Mainly outpatient clinic
Temel 2011,23 Greer 2012,24 Temel 201044	Lung	Within 8 wk of diagnosis	USA	Outpatient-based	Favors PC		Favors PC		Favors PC	Favors PC	Favors PC
Zimmermann 201425	Breast, lung, GI, GU, GYN	Prognosis 6-24 mo	Canada	Outpatient-based	Favors PC	Favors PC		Favors PC	Favors PC
Temel 2016,26 El-Jawahri 201727	Lung, GI	Within 8 wk of diagnosis	USA	Outpatient-based	Favors PC		Favors PC		Mixed findings			Mixed findings
Maltoni 201628, 29	Pancreas	Within 8 wk of diagnosis; prognosis >2 mo	Italy	Outpatient-based	Favors PC		Did not differ			Mixed findings	Did not differ
Groenvold 201730	Solid tumors	Symptomatic based on EORTC-QLQ-C30	Denmark	Outpatient-based		Mixed findings					Did not differ
Nurse-led PC
Bakitas 2009,31 Dionne-Odom 201632	Breast, lung, GI, GU	Within 8-12 wk of diagnosis	USA	APN-led, phone based	Favors PC	Did not differ	Favors PC			Did not differ	Did not differ	Mixed findings
Dyar 201233	Solid tumors	Likely to be referred to hospice within the next 12 mo	USA	APN embedded in oncology	Mixed findings	Mixed findings				Did not differ
Tattersall 201434	Solid tumors	Newly diagnosed metastatic disease; prognosis <12 mo	Australia	RN-led	Did not differ	Mixed findings	Did not differ			Did not differ	Favors no PC
McCorkle 201535	Not clearly specified	Within 100 d of diagnosis	USA	APN-led	Did not differ	Did not differ			Favors PC
Bakitas 201536	Solid and hematologic malignancies	Within 1-2 mo of diagnosis; prognosis 6-24 mo	USA	APN-led, phone based	Did not differ	Did not differ	Did not differ			Did not differ	Favors PC	Favors PC
Vanbutsele 201837	Solid tumors	Within 12 wk of diagnosis or recent progression; prognosis ~12 mo	Belgium	RN-led OP team	Favors PC	Did not differ	Did not differ		Mixed findings		Did not differ
Inpatient
Grudzen 201638	Solid and hematologic malignancies	On admission	USA	IP team	Favors PC	Did not differ	Did not differ			Did not differ	Did not differ
El-Jawahri 2016,39 201740	Stem cell transplantation	On admission	USA	IP team	Favors PC	Favors PC	Favors PC					Mixed findings

Abbreviations: APN, advanced practice nurse; EOL, end of life; EORTC-QLQ-C30, European Organization for Research and Treatment of Cancer Quality-of-Life Questionnaire; GI, gastrointestinal; GU, genitourinary; GYN, gynecologic; IP, inpatient; OP, outpatient; PC, palliative care; RN, registered nurse. ^aThe outcomes are color coded to facilitate interpretation. Green = favored the palliative care group with statistically significant findings; light green = some outcomes significantly favored palliative care group, other outcomes equivocal; orange = no statistically significant difference between the palliative care group and the usual oncologic care group; red = favored the usual oncologic care group with statistically significant findings.

It is noteworthy that there is heterogeneity in trial design among the clinical trials, with variable inclusion criteria, care settings, outcome measures, and timing of assessment. These differences in design, combined with significant differences in the nature of palliative care interventions and the timing and intensity of care delivery, contributed to the variability in study outcomes (Table 1).25, 26, 29-31, 33-39, 44 Although the diversity in trial design makes it more difficult to assess the magnitude of benefit associated with palliative care, it also provides a unique opportunity to ascertain which aspects of palliative care may be most beneficial, particularly concerning the level of comprehensiveness of the palliative care service and the timing of referral.

Palliative care is a highly complex, multidimensional intervention, making it difficult to standardize. Although efforts have been made to define the key domains of palliative care,14, 15 it is less clear who is positioned best to deliver palliative care and how comprehensive the team should be. Furthermore, palliative care has not yet been accredited in some countries, which may contribute further to inconsistencies in its delivery. As shown in Table 1, it appears that studies involving interdisciplinary palliative care teams were more likely to have a positive outcome than those involving nurse-led palliative care (4 of 5 trials vs 2 of 6 trials for the primary outcome).23-40, 44 However, to date, no single study has directly compared interdisciplinary teams with single-practitioner–led models, and further research is needed.

Although earlier referral to palliative care is considered to be better than late referral, the optimal timing of referral has not yet been defined. To date, only one randomized clinical trial (RCT) has attempted to address this question directly. By using a wait-list design, the Project ENABLE III study compared early palliative care (within 8 to 12 weeks of diagnosis) versus delayed (3 months later).36 The primary outcome was measured at 3 months. The investigators also conducted longitudinal analyses and reported no significant difference between the 2 groups in quality of life. However, that study had several limitations complicating its interpretation, including underenrollment and contamination. Moreover, the study intervention was predominantly nurse-led and telephone-based, with referral to an interdisciplinary palliative care team on an as-needed basis.28 Studies that used other designs to address the optimal timing of referral are discussed below.

Meta-Analyses

Summarizing data from the aforementioned trials and others, 3 meta-analyses were published in 2016 of 2017 on the impact of palliative care on health outcomes (Table 2).45-47 All 3 concluded that palliative care was associated with improved quality of life, albeit with a small effect size45-47; 2 also concluded that palliative care was associated with improved symptom control45, 47; none reported a significant improvement in survival. This small observed benefit may be because the studies included in the meta-analyses mostly had small effect sizes and also included trials with variable designs.48 One study further concluded that earlier palliative care was associated with a greater quality-of-life benefit,46although that subgroup analysis included only 6 studies (2 studies of early palliative care25, 44 and 4 studies of nonearly palliative care).

Table 2. Recent Systematic Reviews Comparing Palliative Care and Usual Oncologic Care Versus Usual Care Alone^a

META-ANALYSIS	SETTING	NO. OF STUDIES	NO. OF PATIENTS	QUALITY OF LIFE	SYMPTOMS	MOOD	SURVIVAL	OTHER OUTCOMES
Kavalieratos 201645	Cancer and noncancer	15	2355	Favors PC; SMD, 0.46; 95% CI, 0.08-0.83	Favors PC; SMD, −0.66; 95% CI, −1.25 to −0.07		Did not differ; HR, 0.90; 95% CI, 0.69-1.1	PC was associated consistently with improvements in advance care planning, patient and caregiver satisfaction, and lower health care utilization
	Cancer only	11	1670	Did not differ; SMD, 0.12; 95% CI, −0.02 to 0.27	Did not differ; SMD, −0.14; 95% CI, −0.39 to 0.10		Did not differ; HR, 0.82; 95% CI, 0.60-1.13
Gartner 201746	Cancer and noncancer	12	2454	Favors PC; SMD, 0.16; 95% CI, 0.01-0.31	Did not differ; SMD, −0.38; 95% CI, −0.82 to 0.06
	Cancer only	5	828	Favors PC; SMD, 0.20, 95% CI, 0.01-0.38	Did not differ; SMD, −0.21; 95% CI, −1.35 to 0.94
	Early only	2	388	Favors PC; SMD, 0.33; 95% CI, 0.05-0.61
Haun 201747	Advanced cancer	7	1614	Favors PC; SMD, 0.27; 95% CI 0.15-0.38	Favors PC; SMD, −0.23; 95% CI, −0.35 to −0.10	Did not differ; SMD, −0.11; 95% CI, −0.26 to 0.03	Did not differ; HR, 0.85; 95% CI, 0.56-1.28	RCTs on professional PC services that provided or coordinated comprehensive care for adults at early advanced stages of cancer

Abbreviations: 95% CI, 95% confidence interval; HR, hazard ratio; PC, palliative care; SMD, standardized mean difference; RCTs, randomized controlled trials. ^aThe outcomes are color coded to facilitate interpretation. Green = favored the palliative care group with statistically significant findings; orange = no statistically significant difference between the palliative care group and the usual oncologic care group.

In addition to the heterogeneity among clinical trials, the 3 meta-analyses used different eligibility criteria, resulting in the inclusion of different trials and somewhat variable findings. The review by Kavalieratos et al had the broadest inclusion criteria, including 43 trials in patients with life-limiting illness, for which interventions comprised at least 2 of 8 possible domains of palliative care, as defined by the National Consensus Project for Quality Palliative Care.49 Palliative care was associated with a statistically and clinically meaningful improvement in quality of life overall for the 15 studies included in one meta-analysis, but not when patients with (or without) cancer were analyzed in isolation.45 The review by Gaertner et al included 10 trials of patients with any advanced illness in which the intervention was a multiprofessional palliative care team and reported a marginally larger effect of palliative care on quality of life in patients with cancer than in those without cancer.46 The review by Haun et al included 7 cancer trials that specifically assessed the effects of early palliative care intervention, concluding that quality of life was better in patients with cancer who received early palliative care.47 Ultimately, these meta-analyses underscore the need to conduct further research to identify the optimal model(s) of palliative care delivery in different settings.

Cost Benefits

In addition to improved patient and caregiver outcomes, palliative care is also associated with reduced health care costs. In part, this is driven by the tendency of palliative care teams to minimize investigations, interventions, and hospitalizations at the end of life that not only have questionable benefits but also are expensive.50 Morrison et al reported that an inpatient palliative care consultation was associated with significant cost savings compared with no palliative care, supporting the economic benefit of palliative care for third-party payers and institutions under the Diagnostic Related Grouping payment system.51, 52 Smith et al conducted a systematic review of 46 studies and concluded that palliative care was consistently less costly relative to comparator groups.53 Another systematic review in 2018 reported that a palliative care consultation within 3 days of admission for patients with cancer was associated with a reduction in total direct hospital cost by $4251 (95% confidence interval, $3837-$4664) per hospitalization.54 More high-quality studies are needed to investigate the economic impact from the perspective of different payers (eg, government, insurers, third-party organizations, patients, and family caregivers), in different settings (eg, outpatient, inpatient, home care), and with different models of palliative care (eg, comprehensive teams vs nurse-led care).

Summary

Most RCTs demonstrate that palliative care combined with oncologic care improves quality of life and symptom control.
Clinical trials involving interdisciplinary palliative care teams, instead of nurse-led palliative care, appear to be more likely to be associated with positive findings.
Three recent meta-analyses concluded that palliative care was associated with improved quality of life. However, the effect size was small, which may be related to heterogeneity in trial design.
A meta-analysis examining the timing of palliative care referral supported that earlier referral was associated with greater benefits on quality of life.
Palliative care can improve health care value by reducing costly investigations, interventions, and hospitalizations at the end of life, especially those with questionable benefits.

Defining Key Elements of Palliative Care Delivery: Team-Based, Timely, and Targeted Care

Our critical appraisal of contemporary RCTs above supports the association between specialist palliative care and improved outcomes. Efforts are currently underway to identify the “active ingredients” in this complex intervention and to help standardize the delivery of palliative care. In the section below, we use conceptual frameworks to discuss 4 key questions: What is the right service model? When is the right time? Who is the right patient? And how much palliative care should oncologists provide?

What Is the Right Service Model? The Role of Team-Based Palliative Care

One of the most unique and fundamental aspects of palliative care is its interdisciplinary nature, which allows the team to deliver multidimensional care addressing the complex supportive care needs of patients with advanced cancer. Figure 1 illustrates the interconnectedness of the supportive care needs of patients with advanced cancer. One of the strengths of this interdisciplinary palliative care approach is the shared decision making, responsibility, and leadership to support patients and families. The physician, nurse, psychologist, social worker, chaplain, pharmacist, physiotherapist, occupational therapist, and other allied health professionals each contribute their unique expertise while working together in a cohesive manner to support the patient's goals of care through impeccable assessments, coordinated communication, and multidimensional interventions (Fig. 2). Not all members are required at all times—some may be needed more often than others, and some may form a closer relationship with the patient. In a secondary analysis of the trial by Temel et al,26 Hoerger et al reported that patients who had a greater proportion of visits focused on coping, treatment decisions, and advance care planning (ACP) had better outcomes related to quality of life, chemotherapy use at the end of life, and hospice utilization, respectively, suggesting that each component of palliative care has a specific and complementary purpose.55 Although this interprofessional approach is particularly useful in addressing intense care needs at the end of life, it is also appropriate for patients earlier in the disease trajectory. For example, an interdisciplinary intervention may be particularly helpful to support patients with cancer who are at risk of opioid misuse.56 This teamwork may also help to reduce burnout among palliative care clinicians, which represents an area for future research. An international Delphi study in 2015 reached consensus that, at a minimum, interdisciplinary teams should consist of a physician, nurse, and psychosocial team member.57 The interdisciplinary team may be led by a physician, nurse, or another discipline, with situational leadership depending on the care needs.

Details are in the caption following the image — **Figure 1**
Open in figure viewer PowerPoint

Multidimensional Supportive Care Needs. A patient's supportive care needs can be classified as physical, emotional, spiritual, social, and informational, which often are closely associated with each other. For example, depression can contribute to poor appetite and decreased function, and the reverse could be true. Depression also may impact a patient's decision making, their spiritual well-being, and their relationships with caregivers. This diagram highlights the interconnectedness of supportive care issues and the need for multidimensional assessments and interventions with an interdisciplinary team.

On the basis of the conceptual framework and evidence presented above, models of palliative care involving predominantly a single profession may not be able to support patients who have more complex care needs as comprehensively. For example, there is much variation in the intensity of interdisciplinary palliative care involvement among the nurse-led palliative care trials (Table 1),45-47 although they generally involved a nurse providing palliative care education/support in the front line, with referral to specialist palliative care teams on an as needed basis.36, 37 Studies with limited longitudinal interdisciplinary palliative care engagement often had negative outcomes.34, 35 Properly designed and incorporated, nurse-led interventions may augment the basic level of primary palliative care provided by oncologists, with specialist palliative care reserved for patients in greater distress. Although single disciplinary palliative care should not replace specialist palliative care teams, it may have a role in resource-limited settings, such as rural areas or developing regions. Further research is needed to identify the right intervention for the right setting.

When Is the Right Time? The Rationale for Timely Palliative Care

Although referrals to palliative care often occur at times of crisis (eg, end of life), palliative care is most effective when introduced early. Figure 3 illustrates some postulated mechanisms with which timely palliative care can improve various patient-related outcomes. Appropriate and timely symptom interventions, patient education, and side-effect management may help to minimize emergency room visits and hospitalizations while maximizing patients' function.59 Longitudinal counseling can help to enhance coping strategies in times of stress.55 Prospective observational studies and RCTs have shown that serious illness conversations, ACP, spiritual care, and improved prognostic understanding can help reduce aggressive care at the end of life60-62; all of these are longitudinal processes that require adequate lead-time. By facilitating ACP and providing community-based services, palliative care can support individuals who wish to die at home.63 Figure 4 illustrates that palliative care, at its best, is a form of preventive care.

The optimal timing of specialist palliative care referral remains unclear but likely depends on the individual patient and the health care system. In addition to a meta-analysis suggesting that earlier referral was associated with a greater benefit,46 several nonrandomized studies have also demonstrated the impact of timely palliative care on aggressiveness of care at the end of life.59, 64-66 In a retrospective cohort study, patients who were referred to a comprehensive cancer center more than 6 months before death were compared with those who were referred 6 months or less before death. Earlier referrals were associated with significantly better outcomes in the last 30 days of life, with lower rates of emergency room visits (41% vs 63%; P = .002) and hospitalizations (51% vs 75%; P < .001).59 Jang et al conducted a population-based study to examine the impact of palliative care on aggressiveness of end-of-life care for 5381 patients with advanced pancreatic cancer. Palliative care involvement was associated with less aggressive care, as measured by the use of chemotherapy near death (odds ratio [OR], 0.34), intensive care unit admissions (OR, 0.12), emergency room visits (OR, 0.19), and hospitalizations near death (OR, 0.24); moreover, earlier palliative care was associated with better outcomes.64 Studies from Italy and the United Kingdom examining the effect of palliative care confirmed similar benefits with earlier referral.65, 66

Although early palliative care referral is generally preferred, some investigators have speculated whether it is ever too early. Many contemporary RCTs involved specialist palliative care referral within 3 months of diagnosis of advanced cancer regardless of symptom burden; however, this model of care is currently infeasible given the limited palliative care infrastructure internationally.67, 68 Furthermore, some patients with advanced cancer may have limited supportive care needs around the time of diagnosis and may not require palliative care. Thus, instead of early palliative care for all, we advocate for timely palliative care, selecting the right patient for the right level of intervention at the right time.

One approach to determining the right time involves a Delphi consensus.69 In one study, 60 international experts were asked about the appropriate time to refer patients with advanced cancer to outpatient palliative care. A consensus was defined a priori, with at least 70% of experts reaching agreement. The timing of referral was assessed from 4 different angles: prognosis, time from diagnosis, treatment trajectory, and performance status. Most experts considered that greater than 24 months was too early and identified the optimal timing as a prognosis of 6 to 24 months. Similarly, the ideal timing for referral was within 3 months of diagnosis of advanced cancer if patients had a median survival of 1 year or less, had progressed through at least a single line of systemic therapy, and had an Eastern Cooperative Oncology Group performance of 2 or greater (Fig. 5).69 A survey asked patients with advanced cancer who were referred to outpatient palliative care about their opinion regarding the optimal timing of referral.70 The median survival was 8.5 months, and a majority (n = 144; 72%) reported that the timing of referral was appropriate, with 42 (21%) perceiving that the referral was too late and only 14 (7%) feeling that it was too early.

Timely palliative care is best delivered in the outpatient setting, where patients can receive proactive rather than reactive care.17 The strengths and weakness of various models of palliative care delivery in the outpatient setting are discussed below.

Who Is the Right Patient? A Targeted Approach to Referral

There is currently a gap between the research literature, which recommends routine early palliative care referral, and the reality of clinical practice. If we apply the eligibility criteria in RCTs strictly and adhere to the 2017 American Society of Clinical Oncology guideline, patients with advanced cancer would be referred regardless of symptom burden as long as they meet predefined, time-based criteria (eg, time from diagnosis and/or prognosis) (Table 1),45-47 resulting in universal early referral (Fig. 6A).44, 71 In contrast, oncologists often refer patients selectively based on care needs, which may be delayed because of the underdetection of symptoms and lack of standardized need-based criteria (Fig. 6B).9, 72

The optimal model may be a combination of these 2 extremes, with the use of standardized need-based criteria to trigger a referral for patients who are most appropriate for specialist palliative care in the outpatient setting (Fig. 6C). Similar to cancer-targeted therapy, in which tumors with particular mutations are most likely to respond, palliative care is likely to confer the greatest benefit for patients experiencing or anticipated to have high symptom intensity or other supportive care needs. This would allow for a more personalized approach, matching the scarce palliative care resources to the needs of the individuals. The literature to support this more targeted approach is still emerging. Groenvold et al enrolled patients with solid tumors who were symptomatic based on the European Organization for Research and Treatment of Cancer Core 30 Quality-of-Life questionnaire.30 Although the primary outcome (ie, the most severe European Organization for Research and Treatment of Cancer Core 30 Quality-of-Life symptom item) had greater improvement with palliative care than with usual care, this did not reach statistical significance. Interpretation of the study is complicated because the responsiveness to change of this primary outcome is not well defined. Secondary analysis of other completed RCTs may provide further insights.

How Much Palliative Care Should Oncologists Provide? The Role of Primary Palliative Care

Although oncologists always have a role in the provision of palliative care, one key question is how much they should reasonably be expected to provide.73 Conceptually, palliative care can be categorized into 3 levels based on expertise (Fig. 7). Primary palliative care is basic palliative care provided by the oncology team and primary care physicians; secondary palliative care is defined as specialist palliative care teams working as consultants to address the more complex supportive care needs; and tertiary palliative care involves palliative care as the attending team providing intensive supportive care for the most complex patients, such as in an acute palliative care unit.74 The introduction of nurse-led palliative care models, with an advance practice nurse embedded into an oncology practice, blurs the division between primary and secondary palliative care.

RCTs to date have demonstrated clearly that secondary palliative care integrated with primary palliative care is superior to primary palliative care alone (Tables 2 and 3). However, in resource-restricted circumstances, a fully integrated approach may not be feasible, and a solo practice model in which the oncologist assumes all aspects of supportive/palliative care may be the only option.8, 75

Table 3. Strengths and Weaknesses of Innovative Care Models

MODELS	POTENTIAL STRENGTHS	POTENTIAL WEAKNESSES
Freestanding clinics	Strong evidence base Centralized services Allows for more consistent day-to-day planning and resource utilization Autonomy around clear and consistent referral criteria Customized space for patients with advanced disease Site for education and research in palliative medicine Greater scope for expansion Visible “home” for the palliative care ambulatory service	More startup costs, overheads, and budgetary considerations Developing positive collaborative relationships with the oncology team may require greater attention More clinic appointments for patients







Embedded clinics	Immediate access to palliative care team Minimizes trips to hospital and wait times May facilitate collaboration (clinical and research) between oncology and palliative care teams May help to destigmatize referral Cost-effective in early development of palliative care (shared space, support staff, and other resources)	Difficult to predict volumes and staffing needs from day to day Follow-up visits may be challenging to schedule if needed for palliative care but not oncology Limited scope for expansion Typically room only for a single discipline Consultation may be rushed and completed in a cramped environment Patient and family may be fatigued due to adding on another appointment Providing care across multiple clinics simultaneously may fragment or overstretch services Limited evidence base







Nurse-led practitioners	Capacity to engage in oncology rounds and to foster stronger communication between services Nurse education and mentoring role May be more financially viable than a physician-led model	Reimbursement for nurses A single practitioner cannot replicate the multidisciplinary team involved in holistic palliative care provision It may be difficult to staff multiple clinics with palliative care nurses in larger centers Mixed evidence base and highly heterogeneous models of delivery



Palliative care delivered by oncology teams	Immediate attention to symptom management concerns Care delivered longitudinally from diagnosis to death by the oncology team Necessary when access to palliative care services limited	Time constraints in oncology clinics may limit focus Maintaining dual competencies may be a challenge Lack of access to interdisciplinary team may make comprehensive palliative care provision challenging Expectations of patients may limit ability to conduct timely advance care planning Current evidence does not support this model in isolation




Automatic referral	Standardizes the referral process across clinicians Normalizes the referral process Results in more appropriate referrals, with specialized services provided for those with greatest need Optimizing health care resource utilization by aligning scared palliative care resource to patients most in need	Limited evidence for choice of screening tool, cutoff points for referral Lack of buy-in from patients and/or clinicians may result in low screening rates May trigger unnecessary referrals for symptoms that are transient or could be managed by oncology team

Even under a fully integrated model, oncologists are expected to provide primary palliative care and address basic supportive care needs in the front line,76 partly because there is an insufficient palliative care workforce to support all patients who have advanced cancer and/or significant symptom burden.77 Previous studies revealed that, although a majority of oncologists believe that they are responsible for providing primary palliative care,6 their levels of confidence and interest vary widely.78 For example, solid tumor oncologists perceived themselves as more comfortable with the provision of supportive care than hematologic oncologists (P = .003).79 Primary palliative care delivery by oncologists can also be assessed indirectly by the extent of palliative care education and their knowledge base. Currently, only 20% to 25% of medical oncology fellowship programs in the United States have mandatory palliative care rotations.67, 80 Furthermore, a majority of medical oncology fellows had difficulty with opioid rotation and desired more palliative care education.80

Several groups have undertaken efforts to standardize primary palliative care competencies.81-83 This should start with routine systematic screening, basic management of acute or common issues, and recognition of when a patient needs to be referred to specialized services.84 Standardized referral criteria may further streamline this process and are discussed below. It is also important to differentiate palliative care issues from other supportive care needs best managed by oncologists or other specialists, such as immunotherapy-related toxicities and thromboembolism. More research is needed to define the core competencies and best approaches to educating the next generation of oncologists.85

Summary/Key Points

The interconnectedness of symptoms and supportive care needs necessitates a comprehensive interdisciplinary team to provide multidimensional care.
Although interdisciplinary palliative care teams are ideal, single-disciplinary palliative care may have a role in the provision of primary palliative care, particularly in resource-limited settings.
Palliative care is most effective as a preventive measure when it is introduced early in the disease trajectory. Its roles in this setting include patient education, proper symptom management, longitudinal counseling and spiritual care, enhancing illness understanding, and ACP.
Timely palliative care is associated with improved quality of life and end-of-life care.
Because of scarce health care resources, it is impossible for all patients to be seen by palliative care from the time of diagnosis. Similar to cancer targeted therapy, a more personalized approach to refer patients with higher current or anticipated supportive care needs may result in better outcomes.
Oncologists have an important role in providing primary palliative care, which includes basic symptom assessment and treatment, communication, decision making, and referral to specialist palliative care.

Innovative Models of Care Delivery

The evidence for timely involvement of palliative care and key elements in its delivery are described above. Here, we examine the components of innovative care models for palliative care delivered in the outpatient setting, with an emphasis on highlighting their strengths and limitations. These include freestanding outpatient clinics, palliative care consultants embedded within oncology clinics, nurse practitioner consultants, automated referral to palliative care, and primary palliative care delivered by oncology teams alone (Table 3).

Outpatient Clinics

Timely, integrated palliative care requires contact with patients who have advanced cancer at a time when they remain ambulatory, functionally independent, and engaged with their oncology team in active anticancer treatment. Outpatient clinics provide an ideal setting within which to build trusting relationships with patients and their familie,15; optimize symptom control issues in a timely manner86, 87; and explore ACP in a structured, longitudinal fashion in tandem with changes to the patients' cancer treatment plan.86, 88

In 2009, 59% of National Cancer Institute designated cancer centers and 22% of non-National Cancer Institute-designated cancer centers reported having outpatient palliative care clinics in the United States67; this proportion has likely grown over time.89 Several centers have published their experience with freestanding outpatient clinics.90-95 In most cases, these clinics have begun as single, one-half–day clinics per week and have grown quickly with increasing demand.96-98 Large cancer centers, such as The University of Texas MD Anderson Cancer Center and the Princess Margaret Cancer Center, have clinics that operate daily and offer both booked and urgent same-day appointments. Typically, the core team members providing expertise in the clinic are palliative care physicians and nurses, with other interdisciplinary team members (including social workers, psychologists, spiritual care workers, pharmacists, dieticians, wound care specialists, and occupational and physiotherapists) offering input as required.92, 96, 99 Referrals are received and booked centrally and can be coordinated with oncology clinic visits if that is the patient's preference.100

There is strong evidence demonstrating the benefits of stand-alone clinics (Table 1).23-40, 44 Patients whose initial palliative care contact was in these clinics have improved outcomes related to aggressiveness of care at the end of life (characterized by fewer prolonged hospitalizations, intensive care unit admissions, and emergency department visits in the last month of life and lower rates of in-hospital death) compared with patients seen by the palliative care team as inpatients.59 Robust evidence from several large-scale RCTs has demonstrated clear benefits for patients in terms of improved quality of life,25, 26, 29, 44 with some trials also demonstrating benefits in satisfaction with care,25 symptom management,25 caregiver distress,27, 101 and overall survival.44

In addition, stand-alone clinics offer several advantages (Table 3). They allow for the centralization of interdisciplinary services, with an organized triage process. This allows for better day-to-day planning and efficient use of the multidisciplinary team, which is particularly important with large-volume services and for teams in which members simultaneously cover inpatient and outpatient palliative care services. Clear referral criteria are set, prioritizing urgent same-day referrals for patients with physical or psychosocial distress. The clinic itself may be customized for patients who have complex care needs, with low examining tables, a waiting room (or lack thereof) with an emphasize on privacy, ambient music, and standardized comprehensive palliative care assessments.92, 99, 102 Moreover, the clinic can serve as a specialized setting for education and research.100 This model also solidifies the independent role played by palliative care teams in cancer care rather than being seen as an appendage of individual oncology clinics. To prevent symptom crises proactively, a centralized clinic may also facilitate the coordination of telehealth interventions.103, 104

The main limitations of freestanding outpatient clinics are budgetary and funding restrictions. Consideration needs to be given to this from the outset, with a strong business model and planning for additional resources, space, and clinicians over time. In small centers, it may not be possible to allocate separate space to a clinic that only runs once weekly. Developing positive relationships with referring oncologists may require greater attention compared with embedded clinics.100 Thus, this model is best suited for large cancer centers with an established palliative care program.

Embedded Clinics

Outpatient palliative care clinics also may be embedded directly within oncology clinics.17, 75, 105, 106 A few studies have described successful examples of embedded clinics. In one, a palliative care clinic consisting of a physician and a fellow within a private oncology clinic provided one-half–day per week of consult support. This improved symptom burden and increased referral rates by 87% over a 2-year period; each consultation was estimated to save up to 170 minutes of the referring oncologist's time. Both oncologists and palliative care physicians reported that the close proximity to one another facilitated better integration of practices.105 Cassel et al reported that a palliative care physician within oncology clinics in a rural setting was associated with high levels of patient, family, and referring physician satisfaction.106 In a retrospective cohort study, Einstein et al reported their experience embedding a physician and a chaplain weekly into an oncology clinic that specialized in targeted and immune-based therapies.107 Patients under the embedded model (n = 26) were more likely than those outside of the embedded clinic (n = 88) to be seen by palliative care for longer periods (173 vs 61 days; P < .001) and to be referred to hospice earlier (34 vs 10 days; P = .006).

Embedded clinics offer some advantages both clinically and practically (Table 3). They allow for direct access to the palliative care team, and they minimize the number of hospital trips108 and wait times for patients.17 In contrast to stand-alone clinics,109 embedded clinics also may help to minimize stigma by offering palliative care in the same location as standard oncology care. Embedded clinics may foster improved face-to-face communication and collaboration between oncology and palliative care teams,75, 108, 110 which may spur educational and research opportunities.75 Support staff may be shared between the oncology and palliative care services in an embedded model, again allowing for more cohesive care110 and cost effectiveness. This may be particularly advantageous for newly established palliative care teams that have limited budgets.100

Conversely, this model also has important limitations. Space limitations restrict involvement of the palliative care team to a single discipline, typically a sole physician or nurse, and limit the possibility of expansion.75, 105, 106 Patients with advanced cancer may not wish to add an additional consultation onto their existing oncology appointment because of lack of time or energy.108 The consultation may be rushed and conducted in a cramped environment rather than proceeding at a more relaxed pace in a customized environment. If a palliative care follow-up is required independent of an oncology appointment, this may be challenging to schedule because of space limitations. In large centers where oncology clinics are organized by tumor site, it may be unrealistic to have a physician or nurse in each clinic. Thus a model that relies exclusively on embedded clinics may hamper the ability of the palliative care team to see patients across all tumor sites.17 It may be challenging to plan palliative care resources and manpower, as referrals may be unpredictable from day to day,100 with resources potentially spread across a variety of clinics.75 Because the principles of symptom management and ACP are universal across all tumor sites, the need to subspecialize within individual oncology clinics is likely unwarranted. Finally, there is scant published literature regarding embedded clinics. One study reported poor recruitment (only 3 of 13 patients who were approached agreed to be seen by the palliative care consultant), primarily because of a lack of willingness to engage in an additional consultation or deteriorating health status.111

In summary, the embedded clinic model may be the best available option for centers that are newly developing an outpatient clinic and allows for the promotion of a palliative care model within the oncology team. However, it is not optimal for larger centers where palliative care services are well established.

Nurse Practitioners and Nurse-Led Palliative Care

Nurses specialized in palliative care may enhance the level of palliative care delivery in the oncology setting. Advanced practice nurses or registered nurses may work as specialists embedded within oncology clinics or may be available by telephone or in person on an as-needed basis.

As discussed above, RCTs on nurse-led palliative care have yielded mixed findings (Table 1).31, 33-37 Other studies involving nurse-led models are hampered by limitations in study design that complicate their interpretation.112 In a nonrandomized study, the presence of a palliative care advanced practice nurse within a community cancer center was associated with lower rates of hospitalization (OR, 0.16; P < .01) and improved survival at 4 months (OR, 24.6; P = .02), but there was no improvement in quality of life or symptom management.113 Ferrell et al conducted a large study examining a nurse-led palliative care intervention in which patients with stage I through IV nonsmall cell lung cancer received an initial assessment followed by a discussion at an interdisciplinary team meeting and then nursing education over 4 sessions, and some improvements in quality of life were reported in a before-after comparison.71 Interestingly, the beneficial effect was observed mostly in patients with stage I through IIIB disease instead of those with stage IV disease, although the timing of inception for patient enrollment was not clearly defined. Walling et al embedded a palliative care nurse practitioner in 2 breast medical oncology clinics.114 Compared with 35 oncology clinics that did not have a nurse practitioner, there was greater referral for psychosocial support, ACP, and hospice referral. However, symptoms and quality-of-life outcomes were not assessed.

Nurse-led models may be less expensive to implement than interdisciplinary palliative care teams. They may increase the level of palliative care available at some oncology clinics while allowing for the mentoring of clinic nurses who provide oncology care.115 However, the billing and remuneration aspects of nurse-based models need further clarification.106 Similar to the embedded model, it may be difficult to ensure that each clinic is staffed with a palliative care nurse in larger centers. Because one discipline in isolation is unlikely to allow patients and families to benefit from the attention to all aspects of quality of life, nurse-led palliative care should be regarded as complementary to (rather than replacing) interdisciplinary palliative care teams.

Palliative Care Delivered by Oncology Teams

There are limited data describing optimal models of primary palliative care provided by oncology teams alone. A pilot study was conducted using oncology clinic nurses trained in a care management intervention to facilitate symptom assessment, engage in ACP, provide emotional support to patients and caregivers, and communicate with other oncology team members.116 This model was feasible and acceptable to patients, families, and oncologists; a cluster RCT of this intervention is ongoing.117 Of note, care delivered by oncology teams alone was the control arm in several RCTs demonstrating improved quality of life when a palliative care team was also involved.25, 26, 29, 44 In one of those trials, patients perceived clear differences in the focus (disease vs person/family), motive (managing cancer treatment vs managing symptoms), and model of care (physician-led, time-constrained vs patient-led, flexible) in oncology versus palliative care clinics.16 These findings underscore the complexity of palliative care and indicate that additional education of oncology clinicians is required to more comprehensively address palliative care needs.

This “solo practice” model of palliative care delivered by oncology teams has some advantages (Table 3).8 Patients benefit from the ability to access good symptom support from early in their diagnosis; many may not require secondary palliative care input and can benefit from completely integrated care from diagnosis to death. Oncology teams, in turn, may derive additional professional satisfaction from being able to provide symptom support, especially in areas where access to specialist palliative care teams may be limited.

Potential limitations to the provision of primary palliative care by oncology teams include the time required within oncology clinics to adequately address all aspects of care.105 Maintaining competencies in both active anticancer treatment modalities and symptom assessment and management may be challenging, if not impossible.73 For oncology teams without access to multidisciplinary support, fully holistic care may not be feasible, and the risk of burnout may be increased.118 The needs of caregivers may be overlooked in busy clinical settings, and psychosocial and bereavement support may be challenging to coordinate: palliative care teams may be better able to address these needs.101 Managing transitions in care, including the switch from active anticancer therapy to a purely supportive care approach, may be difficult to balance in a primary palliative care role. In addition, relationships with patients may be based upon expectations of maintaining positivity and hope, which may be impacted by attempts to direct care toward a purely symptom management approach.119, 120

Automatic Referral With Standardized Criteria

In the era of personalized cancer care, patients who have the greatest supportive care needs may be identified and automatically referred to specialist palliative care (Fig. 6C). This approach requires: 1) routine screening of supportive care needs; 2) predefined referral criteria with clinician endorsement; and 3) an automatic referral system in place.17 Importantly, this more targeted approach should not replace clinical judgement, but it can help to inform the treating oncologist to augment care.121

Recent studies suggest that routine symptom assessment in the ambulatory oncology setting improves not only quality of life but also survival.122-124 The Commission on Cancer mandates routine distress screening, with the Distress Thermometer and the Edmonton Symptom Assessment System being used frequently.11, 125, 126 These efforts will likely result in greater awareness of symptom distress and timely, targeted referral.

Ongoing work is being conducted to identify proper standardized criteria, based on care needs and/or timing, to trigger referrals. Patients generally prefer to be referred based on their needs; one study found that those who felt palliative care referral was too early had limited symptom burden at the time of referral.70 Referral based on patient care needs also is supported by the findings from a 2016 international consensus panel. After 3 rounds of deliberation, a panel of 60 experts reached consensus on 11 major criteria for referral to outpatient palliative care.69 Patients who met any one of the criteria would be appropriate for referral. Interestingly, 9 of the 11 criteria were based on patient care needs, and only 2 were time-based (Table 4). Active work is underway to validate the use of these criteria to facilitate referral. In another population-based study of over 11,000 patients, the palliative performance scale (PPS) was used to assign patients as stable (PPS, 70%-100%), transitional (PPS, 40%-60%), end of life (PPS, 10%-30%), or dead. Entry into the transitional state (PPS, ≤60%) was considered a potential indicator for palliative care referral.127 Although a poor performance status may be a good trigger because it indicates greater functional need and shorter survival, the interrater reliability of performance status assessment is suboptimal.128 Patient completion of performance status tools is one option to overcome this, but patients' self-rated scores tend to be worse than those of physicians.129

Table 4. Major Criteria for Outpatient Palliative Care Referral Based on an International Consensus Panel

CRITERIA	CATEGORY
1. Severe physical symptom(s)	Need-based criteria, distress
2. Severe emotional symptom(s)	Need-based criteria, distress
3. Request for hastened death	Need-based criteria, distress
4. Spiritual or existential crisis	Need-based criteria, distress
5. Assistance with decision making/care planning	Need-based criteria, care needs
6. Patient request	Need-based criteria, care needs
7. Delirium	Need-based criteria, neurologic
8. Brain or leptomeningeal metastases	Need-based criteria, neurologic
9. Spinal cord compression or cauda equina	Need-based criteria, neurologic
10. Within 3 mo of diagnosis of advanced/incurable cancer for patients with a median survival ≤1 y	Time-based criteria
11. Diagnosis of advanced cancer with progressive disease despite second-line systemic therapy (incurable)	Time-based criteria

The strengths and weakness of automatic referral models are highlighted in Table 3. In addition to streamlining referral and triaging resources, automatic referral can help to standardize care and normalize the process of referral. There are several challenges with automatic referral. First, implementation of routine symptom screening in the oncology setting requires resources, commitment, and the identification of an appropriate questionnaire, along with cutoffs to trigger referral.126 Second, routine screening inevitably will result in false-negatives and positives, and procedures need to be established to address these issues.130, 131 Third, the palliative care team needs to have adequate resources to handle the increased volume of referrals. Finally, the literature on automatic referral is still evolving, and only a few groups have published their experience.

In a quality-improvement project, the Edmonton Symptom Assessment System was used in a community hospital for distress screening in patients with cancer.11 Patients were assessed by a social worker for triaging if they screened positive, which was defined as at least 3 of 8 target symptoms with an intensity of 7 or greater on a scale of 10. Comparing between the 4-week periods before and after program implementation, there was a significant increase in social work assessments (21% vs 79%; P < .001) and a nonstatistically significant trend toward increased palliative care referral (12% vs 28%; P = .21) among patients who screened positive. Other groups have also reported their preliminary experience related to distress screening to trigger supportive/palliative care referrals.107, 132, 133

Summary/Key Points

There is strong evidence to support stand-alone palliative care clinics to improve patient outcomes. These clinics are ideally staffed with an interdisciplinary team in larger centers. These clinics represent the current standard of care against which other outpatient models should be measured.
Embedded clinics may be more suitable in smaller centers with limited palliative care resources.
Further research is needed to assess the impact of nurse-led palliative care and how this care model interfaces with specialist palliative care teams.
RCTs have found that oncology teams delivering palliative care alone resulted in poorer quality-of-life outcomes versus concurrent care with a specialist palliative care team; however, it is important that all oncologists are trained in providing a basic level of palliative care.
Automatic referral to palliative care may allow for more personalized care. It requires routine screening, standardized referral criteria, and an established palliative care team.
An international consensus study identified 9 needs-based criteria and 2 time-based criteria for referral to outpatient palliative care for patients with advanced cancer.

Conclusions

Patients with cancer have significant supportive/palliative care needs along their disease journey. These needs are growing because of an aging population with multiple comorbidities, increased numbers of patients living with advanced cancer for longer periods, greater emphasis on quality of life, and heightened awareness as a result of more widespread symptom screening. Specialist palliative care teams are well positioned to complement the primary palliative care provided by oncologists toward improving patients' quality of life, symptom control, mood, end-of-life care, and satisfaction.

Evidence from RCTs supports the interdisciplinary nature of palliative care. Palliative care teams provide broad expertise to support the multidimensional care needs of patients and their caregivers. Timely palliative care further enables the team to provide longitudinal pharmacologic interventions, counseling, education, monitoring, and care planning to prevent crises, such as emergency room visits and intensive care unit admissions.

In the era of personalized medicine, the provision of palliative care should be tailored to provide the right level of intervention for the right patient in the right setting at the right time. By anticipating the natural history of advanced cancer and the potential challenges ahead, palliative care can proactively introduce multidimensional measures to improve quality of life throughout the disease course and ensure that end-of-life care is consistent with patients' wishes. Many innovative care models are being developed to foster improved integration between oncology and palliative care teams. There is strong evidence to support stand-alone palliative care clinics that provide interdisciplinary and timely care. Given the scarce palliative care resources, routine screening coupled with automatic referral may allow a more streamlined approach to identifying the patients most likely to benefit from palliative care, akin to the use of molecular testing for targeted therapies.

The provision of palliative care in the oncology clinic can be enhanced by: 1) increasing the delivery of primary palliative care by oncology teams; 2) introducing nurses/practitioners with specialized palliative care training; and/or 3) embedding palliative care physicians/specialists. These models may have an important role in rural areas and/or smaller community centers, but they do not replace the need for specialist interdisciplinary palliative care teams for patients with more complex needs. The evidence to support these models is still limited, and more research is needed to determine how palliative care can further integrate with oncology to personalize supportive care for each patient.

Disclosures

David Hui and Eduardo Bruera are supported in part by grants from the National Institutes of Health (1R01CA214960-01A1 and R21NR016736). David Hui is also supported by an American Cancer Society Mentored Research Scholar Grant in Applied and Clinical Research (MRSG-14-1418-01-CCE) and by the Andrew Sabin Family Fellowship Award. Camilla Zimmerman is supported by grants from the Ontario Ministry of Health and Long-Term Care and the Canadian Institutes of Health Research (152996) and by the Rose Family Chair in Palliative Medicine and Supportive Care. Breffni L. Hannon reports no conflicts of interest.

https://doi.org/10.3322/caac.21490. Available online at cacancerjournal.com.

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Citing Literature

Volume68, Issue5

September/October 2018

Pages 356-376

Improving patient and caregiver outcomes in oncology: Team-based, timely, and targeted palliative care

Abstract

Introduction

Summary/Key Points

Evidence to Support Early Palliative Care

Randomized Controlled Trials

Meta-Analyses

Cost Benefits

Summary

Defining Key Elements of Palliative Care Delivery: Team-Based, Timely, and Targeted Care

What Is the Right Service Model? The Role of Team-Based Palliative Care

When Is the Right Time? The Rationale for Timely Palliative Care

Who Is the Right Patient? A Targeted Approach to Referral

How Much Palliative Care Should Oncologists Provide? The Role of Primary Palliative Care

Summary/Key Points

Innovative Models of Care Delivery

Outpatient Clinics

Embedded Clinics

Nurse Practitioners and Nurse-Led Palliative Care

Palliative Care Delivered by Oncology Teams

Automatic Referral With Standardized Criteria

Summary/Key Points

Conclusions

Disclosures

References

Citing Literature

Figures

References

Information

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