From evidence to practice: early integration of palliative care in a comprehensive cancer center

The American Society of Clinical Oncology (ASCO) recommends that all patients with a diagnosis of advanced cancer be referred to a palliative care team within 8 weeks of diagnosis. The benefits of early integrated palliative care are well recognized; however, there is a lack of consensus to guide operational aspects of a palliative care service within a comprehensive cancer center. In this study, we explore current palliative care referral patterns at an academic cancer center and provide recommendations for operationalizing palliative care services as a program within comprehensive cancer centers in order to adequately meet the needs of patients with advanced cancer. A retrospective chart review of patients with newly diagnosed metastatic cancer or advanced hematologic malignancy referred to the palliative care team at a comprehensive cancer center from January 1, 2021, to October 31, 2021, was conducted. Institutional Review Board (IRB) approval was obtained prior to the initiation of the chart review. A total of 243 patients with newly diagnosed metastatic cancer or advanced hematologic malignancy were included in this review. Patients with gastrointestinal (26%), gynecologic (19%), and thoracic (21%) malignancies constituted 66% of the total cohort. The most frequent reason for referral was pain (52%). In total, 39% of patients were referred within 8 weeks of an advanced cancer diagnosis. ASCO recommends that all patients with advanced cancer be referred to a palliative care specialist within 8 weeks of diagnosis. Of the newly referred patients with advanced cancer, only 39% were referred to the palliative care team within 8 weeks of their diagnosis. This considerable gap suggests the need for a consensus with regard to operationalizing the palliative care team.


Background and significance
Patients with advanced cancer have complex needs that stem from symptoms secondary to cancer and cancerdirected therapies, existential distress related to death and dying, and decision-making regarding end-of-life care [1][2][3].
Addressing these issues and partnering with the patients and their caregivers in a timely manner is of paramount importance. The World Health Organization defines palliative care as "an approach that improves the quality of life of patients and their families facing the problems associated with lifethreatening illness, through the prevention and relief of suffering by means of early identification and impeccable assessment and treatment of pain and other problems, physical, psychosocial and spiritual" [4]. In the context of oncology, palliative care encompasses symptom management, goals of care conversations, hospice, and end-of-life care delivered in a patient and family-centered approach.
The American Society of Clinical Oncology (ASCO) strongly recommends that patients with advanced cancer be referred to palliative care early in the course of their disease trajectory [5]. The National Comprehensive Cancer Network's (NCCN) guidelines also articulate the importance of early integrated palliative care, but the approach and timelines are not well delineated. Despite ample evidence and consensus that early referral to palliative care has a meaningful impact on a patient's quality of life and overall wellbeing, there remains hesitation on the part of the primary oncology teams to refer patients to these services promptly due to misperception [6]. These misperceptions may be due to the notion of palliative care being equated with end-of-life care. In the last two decades, several studies have reported improvement in patient outcomes in the domains of patientreported quality of life, mood, improvement in the management of symptom burden, less aggressive care toward the end of life, and an improvement in overall survival [1,[6][7][8][9].
With the wealth of evidence demonstrating the various benefits of palliative care, it made sense when in 2017 ASCO formally recommended that patients with newly diagnosed advanced cancer should be referred to palliative care within 8 weeks of their diagnosis [5]. While this was a great step forward for the field of palliative medicine, there was little to no guidance on how cancer centers were to meet this recommendation. A survey of cancer centers in 2018 showed that 95% of National Cancer Institute (NCI)-designated cancer centers had outpatient palliative care programs while only 40% of non-NCI-designated cancer centers did [10]. These teams often consist of one palliative care physician, with a supporting advanced practice provider or a registered nurse. The adequacy of these teams to meet the needs of the oncology patients within the practice is not clearly established [11].
In this study, we explore current palliative care referral patterns at an academic cancer center and provide recommendations for operationalizing palliative care services as a program within comprehensive cancer centers in order to adequately meet the needs of patients with advanced cancer.

Methods
A retrospective chart review of patients with newly diagnosed advanced cancer from Monter Cancer Center, Northwell Health Cancer Institute, was conducted. The electronic medical record review included new patient referrals to a single palliative care physician from January 1, 2021, to October 31, 2021. Here we define advanced cancer as metastatic disease for solid tumors and recurrent or refractory disease for hematological malignancies. Of the 340 charts reviewed, 243 patients were identified as having the following characteristics: (1) having a metastatic cancer diagnosis, or a recurrent or refractory hematologic malignancy, and (2) having an assigned primary medical oncologist at the Monter Cancer Center. Patients with previously diagnosed early-stage disease who later developed metastatic disease were also included, with diagnosis confirmed based on the review of the relevant pathology report. Patients were categorized based on the following malignancies: breast, head and neck, thoracic, gastrointestinal, genitourinary, gynecologic, sarcoma, and recurrent or refractory hematologic malignancies. The time to first appointment to the palliative care team was determined by the date the patient was seen by the medical oncologist for their first visit for the advanced cancer diagnosis to the date of the palliative care appointment. The reasons for referral were abstracted from the "chief complaint" section of the office visit note documented by the palliative care specialist. In instances where the patient was referred for more than two reasons, the reason for referral was categorized as "greater than or equal to 2 symptoms." Referrals for "goals of care," "palliative care visit," and "symptom management" were noted as specific reasons for referral provided by the referring medical oncologist. This study was approved by Northwell Health's IRB. Descriptive statistics (frequency counts and percentages) were calculated using Microsoft Excel.

Results
A total of 243 patients with newly diagnosed metastatic cancer or advanced hematologic malignancy were included in this review. In total, 60% of the visits were conducted in person, and 40% were conducted using a tele-medicine platform ( Table 1). Twelve percent of all patients referred were under the age of 50 years, 51% were between the ages of 51 and 70 years, and approximately 37% were over the age of 70 (Table 1). Patients with gastrointestinal (26%), gynecologic (19%), and thoracic (21%) malignancies constituted 66% of the total cohort; patients with recurrent refractory malignancy accounted for 8%. Almost half (45.7%) of these patients were referred within 8 weeks of an advanced cancer diagnosis ( Table 2). The most frequent reason for referral to the palliative care team was pain (52%). Of the 39% of patients who were referred within 8 weeks of their metastatic cancer diagnosis (Table 3), 15% were conducted using tele-medicine. And 30 (12%) patients had more than 2 symptoms listed as reasons in the chief complaint. These included the following patient-reported chief complaints: pain and consideration for medicinal cannabis (10), pain and appetite loss/weight loss (4), pain and cough (1), pain and nausea (1), pain and insomnia (1), pain/appetite loss/ cannabis (1), appetite loss and cannabis (1), chronic pain and cannabis (1) fatigue and cannabis (1), nausea and cannabis (1), neuropathy and cannabis (1); in addition 12% of patients were referred by the medical oncologists for more than one reason; these were symptom management and cannabis (1) and palliative care and pain (1). Also 52% of patients in the entire cohort were referred for pain (Table 3); for the patients referred within 8 weeks of their diagnosis, pain (47%) remained the most frequent reason for referral (Table 4). In this group, 3% of patients were referred for "acute pain" (Table 4); per the chart notes, these patients were referred for an "urgent visit" on the same day as their medical oncology visit.
At the time of the data cutoff, 60% of patients were alive, 32% were deceased, and there was no status known for the remaining 8% of patients (Table 1). In addition, 62% of the patients were alive at least for 6 months after their initial palliative care consultation, and of the total number of deceased patients, 59% were referred to hospice care (Table 1); 51% had their first palliative care consultation 8 weeks prior to their death (Table 5).
There were a total of 2,365 new patient visits at the cancer center for the time period of this study. The study design is limited by the inability to comprehensively collect data for the total number of patients with a new diagnosis of advanced cancer seen by the medical oncologists at the cancer center during the study period. Our approximation is that a total of 10% of patients with advanced/metastatic cancer was referred to the palliative care team. Patients with earlystage cancer, on multimodality treatment regimens, who were referred to the palliative care team for symptom management were not included in this analysis. This early-stage cancer cohort constituted approximately 10% of patients seen by the palliative care team during the study period.

Discussion
The palliative care team at our institution is composed of one palliative care physician, one nurse practitioner, and a part-time registered nurse (RN). Staffing limitations may have precluded early integration of palliative care, with the average wait time for a new consultation being typically 3 to 4 weeks. This delay may contribute to increased hospitalizations for poorly controlled symptoms and potentially cause disruption of cancer treatment regimens. Medical oncologists' perspectives and barriers to timely palliative care were explored by Rhonadli et al. [12]. The majority  of oncologists interviewed agreed that palliative care intervention was important and should be integrated early into the care of the patient; however, many of the same oncologists also expressed challenges in doing so, noting that they referred patients to palliative care for end-of-life and goalsof-care conversations if symptom management became challenging, there were no further options for disease-modifying therapies, or when the patient was deemed as a candidate for hospice care. Physicians also expressed that having difficult conversations, especially surrounding poor prognostication, death, and dying, can be a challenge. Moreover, there was hesitation to refer to the palliative care service for the concern that the palliative care team may contradict or alter the plan of care devised by the oncology team. Patients and practitioners alike have several misperceptions regarding palliative care services. Often these discussions may make patients feel abandoned by their oncologists. Oncology teams need to be well-versed and comfortable in discussing these issues with patients and their families in a comforting, empathetic, and non-apologetic manner. Although the reasons for this are multifactorial, the key drivers seem to be a lack of access to evidence-based resources, relevant training, and organizational support [13]. Clinicians need access to these evidence-based resources and guidelines, training in communication, and other relevant skills to help navigate patients with various literacy levels and diverse cultural backgrounds.
There is a heightened awareness of the need for specialized palliative care teams embedded in the oncology clinics. However, given the shortage of formally trained palliative care specialists [14], it is necessary to ensure that    oncology clinicians are equipped with the knowledge and skills necessary to provide appropriate and timely palliative care services to their patients. This workforce shortage presents a major barrier to broadening access to palliative care. The American Academy for Hospice and Palliative Medicine (AAHPM) has proposed legislation to address this problem [15]. The Palliative Care and Hospice Education and Training Act (PCHETA) would amend the Public Health Service Act to increase the number of permanent faculty in palliative care at accredited medical, nursing, and social work schools, and it would also promote education and research in palliative care and hospice, supporting the development of faculty careers in academic palliative medicine. The passage of this legislation would help grow the palliative care workforce over time [16]. While this is an ambitious and worthy endeavor, it is a long-term solution that will not benefit patients who need palliative care in the present. The benefits of palliative care integration into oncologic care have been well established in the literature; however, there are also several documented barriers to early integration of palliative care. Keeping up with the needs of a growing population of chronically ill oncologic patients requires thoughtful solutions. It is reasonable to expect that primary oncology teams are able to manage noncomplex pain and cancer treatmentrelated symptoms. This is often referred to as primary palliative care or nonspecialist palliative care. For patients experiencing neoplasm-related pain, palliative care referral is appropriate when there are escalating opioid requirements for difficult to manage pain, intolerance of opioids, or when there is a known history of opioid or substance misuse. Multiple uncontrolled symptoms related to cancer and cancer treatment merit palliative care consultation without hesitation. Depending on one's training, comfort level with the management of pain and symptoms is highly variable for the oncology clinician. Clinicians' lack of awareness of the current evidence, consensus, and guidelines for palliative care and the lack of communication skills required to have "difficult conversations" with patients and their families can pose as barriers to providing timely primary palliative care to their patients [17].
In-service teachings and formal didactics on pain and symptom management should be provided to oncology staff on a regular basis. While the responsibility of providing these teachings may often fall upon the palliative care clinician, this is not a reasonable expectation. A potential solution is to have this teaching done by a palliative medicine or oncology fellow. This avenue would benefit not only the audience but also the fellow, who would gain comprehensive knowledge on the topic being taught as well as presentation experience, an important lifelong skill. Alternatively, or perhaps, in addition, teaching modules on common topics such as cancer pain management and chemotherapy-related nausea and vomiting, among others, can be recorded and housed in a readily accessible internal website for asynchronous learning among the oncology clinicians. Ensuring that palliative care is part of the oncology fellowship curriculum will equip oncologists entering the workforce with the tools necessary to meet primary palliative care needs.
Advanced practice providers (APPs: physician assistants and nurse practitioners) can prove to be a valuable resource in meeting the palliative care needs of patients. An educational intervention to provide APPs with the necessary skills and tools can bridge the gap between formal palliative care referral and the provision of palliative care services as part of the routine oncology clinic. With the appropriate training and resources, it is reasonable to expect APPs to initiate GOC conversations. Collaborating physicians should empower APPs to initiate advance care planning conversations in order to continually assess what matters most to the patient and their families and to ensure that treatment aligns with these wishes. Furthermore, RNs and social workers can begin advance care planning by assessing if a health care proxy (HCP) has been designated and advance directives documented. This assessment offers a segue into the importance of establishing a HCP and consideration of advance care planning, which can be a conversation built upon by the primary team at follow-up visits.
A palliative care expert consensus proposed an automated trigger for referral to palliative care clinics based on predefined criteria, in addition to oncology clinician referrals [18]. Electronic health records (EHR) can be employed to extract useful data regarding patients referred for palliative care consultation, such as the reason for referral, time to consultation, and hospital admissions. These data can be used to justify additional resources. For example, if it is noted that the time to consult for acute pain is many weeks and patients are visiting the emergency department for uncontrolled pain in the interim, a case can be made to expand clinic hours and/or hire additional clinicians. Furthermore, clinical decision-making algorithms can be used as triggers for palliative care referral and automated prompts can be embedded to remind the clinical care teams to initiate the referral process.
Outcome measures and ongoing evaluations are critical in ensuring that interventions are aligned with the objective of timely access to palliative care. Patient-reported outcomes, a decrease in utilization of acute/emergency care services for symptom management, and an increase in the utilization of hospice care toward the end of life are some examples of metrics that can be routinely measured. Evaluation of interventions and communication of findings to clinical and operational leaders will ensure ongoing engagement, continuous quality improvement, sustainability, and growth of palliative care initiatives. Given our small data set, life and death trends between patients seen in person versus via tele-visits could not be interpreted, an area meriting further exploration. Of note, the very low referral of patients with recurrent/refractory hematologic malignancy (8%) for palliative care highlights an important disparity that needs to be addressed.

Conclusion
A limitation of this study was the inability to capture the total number of patients with advanced cancer during the study period. However, as reported in the literature, we concur that the number of patients referred to palliative care is far lower than the actual number of patients with advanced cancer. A better understanding of why patients are not referred will help to streamline solutions towards improved referral processes. The use of out of the box solutions such as EHR prompts suggesting referral to the palliative care team at the time of diagnosis would capture more referrals, thus bringing us closer to meeting the ASCO guideline. Although we have been successful in understanding barriers and making a case for early referral to the palliative care team, our progress in finding solutions and operationalizing early referral of patients with advanced cancer has been slow. The need for palliative care has been successfully established at our institution; however, we must find more efficient and large-scale ways to operationalize this process.
There is ample evidence that integration of early palliative care will not only provide timely support to patients and their caregivers as they navigate the much more difficult, complex, and challenging cancer care journey, but it will also lead to an economic benefit to the health care systems, as the patients will incur fewer hospital days, ICU stays, and less aggressive care towards end of life. Despite the evidence, guidelines, and consensus regarding the importance of early integration of palliative care for patients with cancer, the incorporation of palliative care services into oncology practices continues to be a challenge. ASCO's recommendation of early palliative care [5] brings to light additional challenges to the constrained resources as the palliative care team is responsible for meeting the needs for all oncology patients, and not only patients with an advanced cancer diagnosis. Patients with early-stage disease receiving multimodal therapies (e.g., chemotherapy, radiation therapy) have complex symptom management needs requiring palliative care services. Meeting the ASCO recommendation may cause additional strain on the already strained palliative care teams and should be accompanied with guidance for how to operationalize palliative care within outpatient oncology clinics.
The process of transforming evidence into practice will require engagement and action from key stakeholders involved in caring for patients with cancer. Intentional and active engagement of the oncology teams in this process, leaving aside the past held beliefs and perceptions, will ultimately improve patient outcomes. To bring about this change will require active engagement at the organization and the system level to ensure that barriers are assessed, understood, and oncology care providers not only have access to the evidence and guidelines but are equipped with the knowledge and skills to be able to have these conversations with their patients. A bridge between formal palliative care provided by a specialist team, while also equipping the oncology clinicians to provide primary palliative care can be the solution that is needed to ensure the timely provision of palliative care services to patients with advanced cancer. Utilization of APPs to expand the palliative care team provides much-needed access to secondary palliative care amid a workforce shortage. The misconception of palliative care being synonymous with end-of-life care is antiquated, and education of the interdisciplinary team is required to ensure patients have adequate access to this vital specialty. Palliative care aims to provide an "extra layer of support" for patients and caregivers in addition to standard oncologic care and can be provided along with active treatment. It is imperative that the modern definition of palliative care be widely distributed.