Symptom burden and shared care planning in an oncology nurse-led primary palliative care intervention (CONNECT) for patients with advanced cancer

Purpose: Primary Palliative Care (PPC) interventions are needed to address unmet symptom needs within standard oncology care. We designed an oncology nurse-led PPC intervention using shared care planning to facilitate patient engagement. This analysis examines the prevalence and severity of symptoms reported by patients and how symptoms were addressed on shared care plans. Methods: Secondary analysis of a cluster randomized PPC intervention trial. Adult patients with metastatic solid tumors whose oncologist ‘would not be surprised if the patient died within a year’ were included. Twenty-three oncology nurses received PPC training and conducted up to three monthly visits with patients. Symptom prevalence and severity were assessed prior to each visit using the Edmonton Symptom Assessment Scale (ESAS; 9 symptoms ranked 1-10 with scores ≥ 4 indicating moderate severity). Nurses collaboratively developed treatment strategies with patients, targeting the most bothersome symptoms for improvement. Results: Among 571 nurse-led PPC visits with 235 patients, the most prevalent and severe symptoms were tiredness (reported at 86% of visits; ESAS ≥ 4 in 55% of visits), low sense of well-being (78%; ESAS ≥ 4 in 38%), and poor appetite (69%; ESAS ≥ 4 in 42%). Moderately severe symptoms were addressed on shared care plans ranging from 4% (drowsiness) to 35% (tiredness) of the time. Symptom management plans developed by PPC-trained oncology nurses primarily focused on non-pharmaceutical interventions (70%) compared to pharmaceutical interventions (30%). Conclusion: The symptoms that patients report most frequently and as most severe on shared care plans were addressed less frequently than expected. Further research is needed to understand how primary palliative care interventions can be designed to more effectively target and improve bothersome symptoms for patients with advanced cancer.


Introduction:
The addition of specialty palliative care to standard oncology care improves quality of life and symptom burden for patients with advanced cancer [1][2][3][4].Despite these demonstrated bene ts, it is not feasible for every patient with serious illness to receive specialty palliative care due to specialist workforce shortages [5].Primary palliative care, or the provision of palliative care by non-specialists, is a potential alternative [6,7].However, primary palliative care interventions must be effectively designed to address key domains of quality palliative care [8].A recent analysis found that primary palliative care interventions were less likely than specialty palliative care interventions to address physical needs and did not demonstrate an impact on symptom burden [9].An enhanced understanding as to how primary palliative care approaches address unmet symptom needs is necessary so that future primary palliative care trials can effectively target and improve symptom burden.
The Care Management by Oncology Nurses (CONNECT) intervention trained and supported existing oncology infusion room nurses at community cancer centers to provide primary palliative care along with standard oncology care.Symptom assessment and management was a key component of this primary palliative care approach [10].To maximize patient involvement, infusion room nurses completed shared care plans with patients to identify and target patients' most bothersome symptoms during intervention visits.In a recently completed cluster randomized trial, the CONNECT intervention did not signi cantly improve overall symptom burden at three months when compared to standard oncology care, although there was evidence of a dose effect, with patients who received the full intervention experiencing greater symptom improvements [11].
In this analysis, we sought to report the prevalence and severity of symptoms experienced by patients with advanced cancer during primary palliative care visits, describe the frequency with which symptoms were addressed by oncology infusion room nurses using shared care plans, and categorize strategies used to manage these symptoms.For this study, we used a dataset of 571 primary palliative care visits conducted with patients with advanced cancer from the CONNECT trial [11].This analysis will inform future development of primary palliative care interventions aimed at improving symptom burden in patients with advanced cancer.

Methods:
Overview: This study is a secondary analysis of data collected during the CONNECT trial (ClinicalTrials.govidenti er: NCT02712229).This trial enrolled patients with advanced cancer at 17 community oncology clinics in Western Pennsylvania from July 2016 through February 2020.Full details and results of the study have been published previously. 11This is the rst analysis to focus on symptom assessment and management.

Participants:
Eligible patients were adults (>21 years old) with a diagnosis of metastatic solid tumor and an Eastern Cooperative Oncology Group (ECOG) performance score ≤2 (ambulatory, capable of self-care, and active for ≥50% of the day), [13] who were planning on receiving ongoing care from the cancer clinic participating in CONNECT and for whom their oncologist "would not be surprised" if they died within the next year [11,12].Patients were ineligible if they were unable to read and write, unable to provide consent for treatment, or had a hematologic malignancy [10].All participating patients provided written informed consent.Patients enrolled in the intervention arm who completed at least one CONNECT visit with a shared care plan were included in this analysis.

Intervention:
CONNECT recruited and trained existing oncology infusion room nurses.Training consisted of an immersive (intensive) three-day instruction on evidence-based palliative care strategies to improve quality of life and symptom burden, with role-playing scenarios to practice newly learned skills.Nurses were taught to develop treatment plans informed by a palliative care symptom management resource guide, as well as discussions with the patient about what had or had not worked for them in the past, their expectations and goals, and their preferences.After training and throughout the intervention, nurses received on-going support from an experienced nurse project manager.
CONNECT nurses focused on providing four key components of primary palliative care: symptom assessment and management, emotional support, advance care planning, and care coordination.
CONNECT nurses met with monthly with patients for three months, before, after or proximal to regularly scheduled oncology visits.When an in-person visit was not possible, nurses conducted the visit via a scheduled phone call.Nurses communicated with participating patients' oncologists after each CONNECT visit to discuss details of the encounter including patients' view of their illness, symptom severity and SCP treatment plans.This collaboration was particularly important when nurses felt pharmaceutical interventions were most appropriate to address patients' symptom needs.
During their visit, nurses reviewed the ESAS, elicited the patient's symptom needs, and came to an agreement on which symptom(s) to target and address on the shared care plan (SCP).Shared care plans were based on collaborative care models for managing chronic illness across various primary care settings (see appendix) [20,21].Nurses completed SCPs with patients during each intervention visit.
Shared care plans facilitated patient engagement in discussions regarding symptom burden and promoted effective self-management strategies.Nurses recorded ESAS symptom severity for the most bothersome symptom(s) and corresponding treatment plans on the SCP.At the end of the visits, nurses provided a copy of the SCP to the patient and kept the original to be discussed with the patient's oncologist and referenced at subsequent CONNECT visits.SCPs guided longitudinal discussions of symptom burden and management across CONNECT visits.
All enrolled patients completed demographic questionnaires at study enrollment, including age, sex, race, time since diagnosis, and cancer type [10,11].

Analysis:
ESAS scores are presented as a continuous variable (mean ± standard deviation) for each intervention visit and overall, across all three intervention visits.Symptom prevalence was determined by considering a symptom 'present' when its ESAS score was score ≥ 1 and 'moderately severe or greater' when the ESAS score was ≥ 4. Symptoms were considered "addressed" if they appeared on the patient's shared care plan for that visit.
To establish uniform data abstraction parameters, two study staff members independently reviewed each SCP to determine what symptoms were addressed and categorize written treatment plans.If more than one symptom was included on a SCP, all were considered addressed during that visit.
We categorized treatment plans as pharmaceutical or non-pharmaceutical and reported frequencies (percentages) for these categories.Pharmaceutical treatment plans included new prescription or over-thecounter medications and medication dosage or frequency changes.Non-pharmaceutical treatment plans included suggested behavior modi cation, psychosocial change, dietary change, referral to additional healthcare provider, and homeopathic remedies.If a treatment plan did not t clearly into one of the decided categories, it was categorized as both (e.g., referral to a specialist provider for a medication adjustment).If addressed symptoms had multiple treatment plans, each plan was categorized individually.When adjustments were made to treatment plans from a previous visit, that symptom was considered addressed again during the subsequent visit.

Results:
Among 336 intervention arm patients enrolled across 9 oncology practices, 235 completed at least one CONNECT visit with a shared care plan and were included in this analysis.The patients included in this analysis had a mean age of 68.4 (SD 9.9) years, were near evenly split by gender (53% female), and were mostly Caucasian (>94%) and non-Hispanic (99%).The most common cancers that were treated included lung (40%), gastrointestinal (28%), genitourinary (16%), and breast (12%) (Table 1).
Treatment strategies used to address individual symptoms are shown in Table 3. Poor sense of wellbeing, poor appetite, drowsiness, and tiredness were addressed with non-pharmaceutical interventions in more than 80% of primary palliative care visits.Nausea and pain were predominantly managed with pharmaceutical treatment plans.Inclusion of a pharmaceutical intervention on a treatment plan was less common overall compared to inclusion of a non-pharmaceutical interventions (Table 3).

Discussion:
In this secondary analysis of an oncology nurse-led primary palliative care intervention, we identi ed the frequency and severity of symptoms reported by patients with advanced cancer and assessed the frequency and manner with which these symptoms were addressed on shared care plans.While palliative care is often thought of as primarily addressing pain in advanced cancer, we observed that the most commonly reported ESAS symptoms were tiredness, low sense of well-being, and poor appetite.These symptoms were also ranked as the most severe.The most common and severe symptoms were addressed infrequently on SCPs, however, at just over half of visits in which they were present.Particularly, low sense of well-being was commonly reported as moderately severe, yet infrequently addressed.Nurses predominantly facilitated non-pharmaceutical interventions to address patients' reported symptoms.
Our reported prevalence and average severity of ESAS symptoms is similar to previous investigations of patients with advanced cancer in palliative care settings [18,22,23].Tiredness (fatigue) is consistently reported to be highly prevalent in patients with advanced cancer [23][24][25].In addition, our nding of average ESAS symptom severity as low-to-moderate is consistent with previous work [26].Knowledge of which symptoms are reported most frequently by patients with advanced cancer is key in designing interventions to improve symptom burden.Our ndings add to the growing body of literature demonstrating certain symptoms with low-moderate severity remain highly prevalent in patients with advanced cancer and associated with poorer quality of life [27][28][29][30].
Symptoms that patients ranked as moderately severe on the ESAS were frequently not addressed on SCPs.This was particularly true for low sense of wellbeing, drowsiness, and depression.These ndings suggest that oncology nurses may feel better equipped to address physical symptoms than psychological symptoms.Though trainings provided nurses with skills for symptom management, CONNECT nurses may have felt they had inadequate time, training, or tools to effectively manage certain psychological symptoms.Additionally, physical symptoms may have been more straightforward to discuss with oncologists, leading to prioritization.In a separate focus group study, oncology nurse reported that patients' lack of emotional disclosure impacted the provision of psychosocial care [31].Similar themes may also have limited nurses during CONNECT intervention visits.
It is also possible that the symptoms patients rank as most severe on an ESAS may not be the symptoms they brought up to discuss with the oncology nurse.For instance, if patients felt their oncology team was not equipped to handle their depression or low sense of well-being, they may not identify it when asked.
Conversely, patients may have existing social or community resources they feel are su cient in managing their psychological symptoms.Some patients may also fear that discussing certain symptoms with a member of their oncology team will impact their ongoing cancer treatment.Previous work has demonstrated that although patients with cancer may perceive issues as important (e.g., advance care planning), they may be unwilling to raise those issues to their providers [32].Furthermore, sociocultural norms and the stigma surrounding mental health and its treatment may account for a reluctance of some patients to choose psychological symptoms to be addressed.Interestingly, we found that the majority of treatments facilitated by oncology nurses to address ESAS symptoms were non-pharmaceutical.This nding may partially result from the intervention being led by non-prescribing clinicians.While the oncology nurses were asked to follow up with oncologists to discuss treatment plans and needed prescriptions, they may have prioritized non-pharmaceutical approaches that could be offered without oncologist involvement, e.g., behavior, psychosocial, dietary, or homeopathic recommendations.However, it is also the case that we have effective pharmaceutical interventions for certain symptoms (e.g., nausea and pain), but limited pharmaceutical options that are effective in managing the symptoms most frequently endorsed by patients with advanced cancer (e.g., tiredness, low sense of wellbeing, and poor appetite).

Implications & Next Steps:
Our ndings suggest that nurse-led PPC interventions may require additional resources and support for oncology nurses to effectively manage the symptoms of patients with advanced cancer.Future nurse-led primary palliative care interventions should be designed to place special emphasis on training and equipping oncology nurses with the skills and resources they need to identify and effectively manage patients' burdensome symptoms.Interventions led by non-prescribing clinicians should be designed to ensure treatment collaboration with prescribers.Additional consideration should be made for assessing and improving patients' overall wellbeing.Normalizing discussion of psychological symptoms across members of the oncology team may allow patients to feel comfortable broaching these concerns.

Limitations:
This secondary analysis has several limitations.Our results are exploratory in nature and intended to be hypothesis-generating.Although the ESAS was administered at each visit, we were unable to identify symptoms that may have been discussed and addressed during visits but not included on SCPs.We also do not know the extent to which SCPs truly addressed symptoms that were most bothersome to patients.Lastly, our sample population is mostly Caucasian, non-Hispanic, and from Western Pennsylvania, which limits overall generalizability.

Conclusion:
In conclusion, we found the symptoms that a population of patients with advanced cancer rank as most severe on an ESAS are not always the symptoms addressed by primary-palliative-care-trained nurses in shared care plans.Further research is needed to understand how primary palliative care interventions can be designed to effectively target and improve symptom burden in patients with advanced cancer.reported at moderate severity of greater ≥ 4) and addressed by nurses.Symptoms were considered addressed if they were recorded on a shared care plan with a treatment plan during at least one intervention visit.The most prevalent symptoms included tiredness (reported at 85% of visits), wellbeing (78%), and poor appetite (69%).The most prevalent moderately severe symptoms included tiredness (reported at 55% of visits), poor appetite (42%), and low sense of wellbeing (38%).The most frequently addressed symptoms were tiredness (addressed at 35% of visits), poor appetite (20%), and pain (16%).Drowsiness and nausea were addressed most infrequently (4% and 5%, respectively).

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Figure 1 Percentage
Figure 1

Table 2 .
: Edmonton Symptom Assessment Score (ESAS) Severity Reported by Patients with Advanced

Table 3 .
Strategies Employed by Oncology Nurses to Address Symptoms during N=571 *Total > 571 because > 1 symptom addressed at some visits