Patients with advanced cancer: when, why, and how to refer to palliative care services

Palliative care (pc) is a fundamental component of the cancer care trajectory. Its primary focus is on “the quality of life of people who have a life-threatening illness, and includes pain and symptom management, skilled psychosocial, emotional and spiritual support” to patients and loved ones. Palliative care includes, but is not limited to, end-of-life care. The benefits of early introduction of pc services in the care trajectory of patients with advanced cancer are well known, as indicated by improved quality of life, satisfaction with care, and a potential for increased survival. In turn, early referral of patients with advanced cancer to pc services is strongly recommended. So when, how, and why should patients with advanced cancer be referred to pc services? In this article, we summarize evidence to address these questions about early pc referral: ■ What are the known benefits? ■ What is the “ideal” pc referral timing? ■ What are the barriers? ■ Which strategies can optimize integration of pc into oncology care? ■ Which communication tools can facilitate skillful introduction of pc to patients?


INTRODUCTION
Palliative care (pc) focuses on "the quality of life of people who have a life-threatening illness, and includes symptom management, skilled psychosocial and spiritual support" to patients and loved ones 1 . Palliative care has been found to enhance quality of life and satisfaction with care for patients with advanced cancer, to reduce chemotherapy use near the end of life, and potentially to increase survival [2][3][4][5] . Nonetheless, suboptimal pc referral remains a barrier to high-quality care in advanced cancer 6 . An authoritative report stated that two thirds of patients requiring pc services accessed them only during their final hospitalization 6 . Given its associated benefits 2,3 , early pc referral for patients with advanced cancer is strongly recommended 7 .
In this article, we address these questions about pc referral: ■ What are the known benefits? ■ What is the "ideal" pc referral timing? ■ What are the barriers? ■ Which strategies can optimize integration of pc into oncology care? ■ Which communication tools can facilitate skillful introduction of pc to patients?

QUESTIONS ABOUT EARLY PC REFERRAL Benefits
The exponential advances made in cancer treatment do not appear to have been matched by equivalent advances in supportive interventions, leaving patients with greater psychological and physical symptom burdens from their cancer therapies 8 . Oncologists likely feel genuine concern for the psychological well-being of their patients, but findings suggest that they lack the time to comprehensively screen for distress 9 . Early integration of pc might not only improve physical symptom control, but also enhance psychological health 5,10 . Early referral to pc for patients with advanced cancer has also been associated with enhanced quality of life by increasing the patient's understanding of their disease and anticipated prognosis, and facilitating coping and advance care planning [11][12][13] . Moreover, a recent report from the Canadian Partnership Against Cancer indicated that nearly 1 in 4 cancer patients experience 2 or more hospital admissions in the last 4 weeks of life, suggesting a need for an improved process of referral to pc services 6 . Evidence has shown that early pc referral is associated with decreased use of chemotherapy and fewer hospitalizations near the end of life 4,12 . Worthy of mention is that fact that no harmful outcomes have been identified from early involvement of the pc team 7 . Integration of interdisciplinary pc services into the routine oncologic care of patients with advanced cancer is therefore recommended 7 .

"Ideal" PC Referral Timing
Several variables have been used to determine the most opportune time to refer patients to pc services, including cancer trajectory, disease extent, response to treatment or lack thereof, and anticipated prognosis.
With respect to cancer trajectory, the World Health Organization describes pc as "applicable early in the course of illness, in conjunction with other therapies that are intended to prolong life" 14 . Being poorly defined, the term "early" can lead to differences in interpretation about when pc referral is warranted. Similarly, considerable variation in the definition of the term "early" has been described, ranging from time of diagnosis of advanced disease, to shortly after or upon failure or discontinuation of curative treatments, to the period just before expected death (in months) [15][16][17][18] . Those variations could contribute to delays in the more prompt integration of pc services into patient care.
Another described marker for pc referral is disease extent. The U.S. National Cancer Institute defines advanced cancer as "cancer that has spread to other places in the body and usually cannot be cured or controlled with treatment" 19 . That definition has its limitations, in that certain malignancies (such as brain cancers) are associated with poor prognosis even in the absence of distant metastases. Likewise, given that decreased rates of aggressive treatment have been reported to be a benefit of early pc referral, the use of treatment failure or discontinuation as a referral criterion appears to be unsuitable.
Lastly, estimating the prognosis of cancer patients can be an imprecise and ambiguous process, with clinicians tending to overestimate survival 20 . Making use of anticipated prognosis such as "less than 3 months" as an indicator for pc referral is therefore unreliable. The American Society of Clinical Oncology's recently published guideline about the integration of palliative care into standard oncology care recommends that "inpatients and outpatients with advanced cancer should receive dedicated palliative care services, early in the disease course, concurrent with active treatment" 7 . Referral to pc for patients with advanced cancer should therefore occur as early as possible in the cancer trajectory, rather than be reserved until the last days of life.

Barriers
In addition to heterogeneity in pc delivery models 3,21,22 , specific patient-flow obstacles have been described as barriers to pc referral. Those obstacles include lack of referral criteria and clearly defined timing for pc referrals 23,24 .
Palliative care is a unique field, in that referrals are seldom based on objective criteria-contrary to, for example, an identified gastrointestinal bleed as a clear criterion for gastroenterology consultation. Rather, pc referrals are heavily influenced by patient needs 24 . Although anticipated short prognosis has been reported to be an objective pc referral criterion, it has evident flaws, given that patients are often referred too late in the course of their illness 25 . Health provider-related obstacles have also been identified as barriers to pc referral. Those obstacles include the perception that pc is a service that exclusively provides end-of-life care 26 and a disinclination on the part of oncologists and other professionals to refer patients to pc 27 . Moreover, physician reluctance to engage in discussions about expected prognosis with patients also contributes to delayed pc referral 26 .
In addition to end-of-life care, pc provides a wide array of services, including cancer treatment-related symptom management and psychosocial interventions, which have been shown to benefit patients and family members alike 2,28,29 . Further educational initiatives targeting oncologists and cancer care professionals are therefore urgently needed and show promise in optimizing access to pc services for patients 27,30 .

Strategies
Creating standardized referral pathways, classifying oncology patients into "low versus high" categories with respect to symptom burden, and adopting an integrated cancer care delivery model have been proposed as strategies to improve referral to pc services for patients. The establishment of standardized pc referral pathways to optimize patient flow has been widely recommended 23,24,31 . Hui et al. 24 identified the following 6 recurrent pc referral criteria as benchmarks toward the development of standardized referral pathways: physical symptoms, disease trajectory, prognosis, performance status, psychosocial distress, and end-of-life care planning. Advocacy for clearly defined pc referral criteria as a means to facilitate objective assessment of programs and to guide policymaking has been described 24 . Referral guidelines should take into consideration specific characteristics, given that recent studies have highlighted benefits of pc referral based on the patient's cancer type, sex, and age 9,32 . Lastly, for the referral pathways to be effective, routine and seriated evaluations of the patient's symptoms and consideration for their disease course appear to be of paramount importance 23,31 .
Moreover, categorizing individuals as either low-or high-burden patients could be another strategy for referring patients to pc services when the existing infrastructure might not be capable of receiving universal early pc referrals 33 . "High-burden patients" [those experiencing treatment failure, physical or emotional distress (or both), and interpersonal conflicts] might benefit most from early pc involvement and could therefore be prioritized for referral 33,34 . However, caution should be exercised when attempting to categorize patients in such a manner, given that "high-burden, low-burden" criteria would fail to identify patients with earlier-stage cancer requiring a referral to pc services 22 .
Lastly, integrated cancer care models appear most promising in introducing pc services early in the disease trajectory. Bruera and Hui 34 described three conceptual models to optimize integration of pc services in oncology care: the oncologist solo-practice model, in which the oncologist attempts to deliver the entirety of cancer management, including supportive and palliative interventions; the congress practice model, in which several consultants are independently involved in a patient's care and which is associated with risks of costly and fragmented care; and the integrated care model, in which oncologists involve pc teams early on to collaborate closely in patient care. The integrated care model allows for the simultaneous delivery of cancer treatments and optimal management of cancer-related symptoms and problems, which are both essential and complementary to comprehensive cancer care. However, implementation of the integrated care model into the clinical setting can be limited should its adoption by the referring physicians be suboptimal 34 . Given that pc is a critical component of care that focuses on quality-of-life concerns and caregoal preferences, all efforts should therefore be made to integrate outpatient and inpatient pc services into traditional oncology care 7 .

Communication Tools
Given the nature of their profession, physicians are routinely tasked with disclosing unfavourable health information to patients 35 . Disclosing bad news can be a demanding responsibility, particularly in cases in which treatment options are limited or no longer available 36 . Oncology providers often have apprehensions about discussing pc referral with their patients, because they fear that such referral might be perceived as a sign of hopelessness or might cause depression 37 . Nonetheless, professional ethics and legal obligations oblige physicians to inform patients about any information they request about their disease, treatment plan, and prognosis. Moreover, providing accurate information about prognosis and care plans to patients, whether positive or negative, does not influence hope in patients with advanced cancer 37 . On the contrary, evidence has shown a patient preference to be informed about their anticipated prognosis 37 , and that awareness of prognosis is associated with improved coping and future planning, and increased trust and satisfaction with care [18][19][20] . That said, the manner and ways in which difficult news is related to patients are of critical significance. To skillfully introduce pc to patients, the application of communication tools such as the use of metaphors and communication models can be helpful in guiding difficult conversations associated with pc referrals.
Core communication tactics such as empathic words and active listening can be supplemented with metaphors to facilitate end-of-life conversations 38 . When initiating a conversation about pc service referral with a patient, the "taking a road trip" metaphor can be helpful (Figure 1). In the metaphor, the cancer trajectory is compared to taking a road trip, and the goal is to arrive at destination-that is, to treat the cancer. Some drivers focus solely on arriving at their destination and do not preoccupy themselves with comfort and safety features such as the seatbelt, spare tire, or seat cushion. Other drivers benefit from those features along the ride, such that they can get to their destination in a safer, more comfortable manner. Drivers who opt for the comfort and safety features are better equipped to pursue their goals. Similarly, pc teams can provide physical and psychosocial symptom control by acting as a cushion to help patients throughout their cancer journey. Palliative care services can be compared to robust roadside assistance program that provides security during a road trip 38 . When skillfully used, the metaphor can enhance a patient's understanding and guide future care planning 38 .
Another communication tool useful for facilitating the introduction of pc to patients is the brief and practical spikes model for breaking bad news 40 . The spikes model has four goals: first, to collect information determining the patient's understanding, expectations, and readiness to receive difficult news; second, to give simplified and clear information in keeping with the patient's preferences; third, to acknowledge and support the patient's emotional reactions to the news; and fourth, to formulate a care plan in a joint effort with the patient 40 . Those goals can be attained by realizing the 6 steps of the spikes model, which are setting up the interview, assessing the patient's perception, obtaining the patient's invitation, giving knowledge and information to the patient, addressing the patient's emotions with empathic responses, and strategizing and summarizing 40 . In addition to those 6 steps, we propose the inclusion of a final step called "self-care," because difficult conversations are often described as distressing and unsatisfying by physicians 41 . Engaging in "self-care" measures such as mindful meditation and reflective writing can be helpful in managing difficult conversations and could help to prevent compassion burnout 42 . Table i presents a proposed modified spikess model, which can be applied in clinical settings when engaging in discussions about disease progression, which often precede the referral of patients with advanced cancer to pc services.

SUMMARY
Palliative care services extend beyond end-of-life care. Essential elements of pc include screening for and managing cancer-related symptoms, providing psychosocial care to patients and loved ones, providing education and support with respect to cancer and the patient's anticipated prognosis, and assisting in medical decision-making and advance care planning. Patients with advanced cancer should be referred to pc teams early in the course of their disease and should receive inpatient or outpatient pc services in conjunction with their usual oncologic care.

Key Points
■ Early referral of patients with advanced cancer to pc services is recommended.  40,a Step Activities S Setting up the interview ■ Organize for some privacy.