Background
Palliative care is defined as multidisciplinary care that increases quality of life (QoL) for patients with a life-threatening illness.1,2 Originally provided mainly at the end of life, palliative care is now acknowledged to be relevant throughout the illness trajectory, concurrent with treatments aimed at prolonging life.3,4 There is evidence from randomized controlled trials and meta-analyses that early palliative care (EPC) improves QoL and symptom control in patients with advanced illness, especially in advanced cancer.5–10 As a result, ASCO clinical practice guidelines recommend routine EPC using dedicated palliative care services for patients with advanced cancer.11
Despite this evidence, routine EPC has not been widely implemented, nor is it possible in all settings.12,13 Given widespread international shortages of specialized palliative care professionals,14,15 EPC should ideally be triaged to those in greatest need while those with mild symptoms receive primary palliative care through oncologists and family physicians.3,4 However, oncologists have variable referral practices, with most referring to palliative care late in the disease course.16,17 Although patients with the greatest palliative care needs are those with the most severe physical and psychological symptoms,18–20 these patients are not the most likely to request palliative care services19 and are often unaware that they exist.21,22 There have been previous successful trials of distress screening with linked interventions23–26; however, none have coupled symptom screening with an EPC intervention.
The primary aim of this single-arm phase II trial was to assess the feasibility of a novel intervention—Symptom screening with Targeted Early Palliative care (STEP)—for patients with advanced cancer. Secondary aims were to assess whether STEP identified patients with worse QoL and other patient-reported outcomes (PROs), and whether screen-positive patients who received EPC had better outcomes over time than those who did not receive EPC (ClinicalTrials.gov identifier: NCT04044040).
Methods
Setting and Participants
The trial took place at the Princess Margaret Cancer Centre, a comprehensive cancer center that is part of the University Health Network (UHN) in Toronto, Ontario, Canada. The center has a palliative care program consisting of an outpatient palliative care clinic, an inpatient consultation service, and an acute palliative care unit.27 In the palliative care clinic, EPC is provided by specialized palliative care physicians and nurses, with a wider multidisciplinary team available.28 Patients are referred to the palliative care clinic by medical, radiation, and surgical oncologists or by other physicians at the UHN (eg, psychiatrists, internists).
In Ontario, routine symptom screening at all outpatient visits was initiated in 200629 and has been mandatory at all 14 cancer centers since 2008.30,31 Patients complete the Edmonton Symptom Assessment System-revised (ESAS-r)32 on computers or tablets in clinic waiting areas before appointments.33 Scores are available for review and potential intervention by oncologists and oncology nurses.
Participants were recruited from 5 medical oncology site groups: lung, gastrointestinal, genitourinary, breast, and gynecologic. Research staff screened outpatient clinic lists to identify potentially eligible patients, discussed these patients with their oncologists to confirm eligibility, and approached eligible patients for consent. Eligible patients were adults (aged ≥18 years) with advanced cancer (stage IV; hormone-refractory for those with breast or prostate cancer, and stage III disease was included for lung and pancreatic cancer), an ECOG performance status of 0 to 2, and an estimated prognosis of ≥6 months, as assessed by their primary oncologist. Exclusion criteria were insufficient English literacy to complete questionnaires, poor cognitive status (Short Orientation-Memory-Concentration score <20 or >10 errors),34 and current palliative care team involvement. The study was approved by the Research Ethics Board of the UHN, and all patients provided written informed consent.
STEP Intervention
STEP consisted of symptom screening at every outpatient visit using the ESAS-r, with targeted EPC referral according to an algorithm based on symptom severity (Figure 1). The ESAS-r assesses the severity of 9 common cancer symptoms (pain, fatigue, drowsiness, nausea, anxiety, depression, appetite, dyspnea, and well-being) using 11-point numerical rating scales with anchors of 0 (absent or best) and 10 (worst); these are summed for the ESAS-r Distress score.32 Moderate to severe scores for ≥1 symptoms (≥4/10 for pain, nausea, dyspnea, depression, anxiety; ≥7/10 for fatigue, appetite, drowsiness, well-being) triggered an email to the palliative care triage nurse, who contacted these “screen-positive” patients to further assess symptom severity, explained the relevance of EPC, and offered a palliative care clinic appointment.35–37
STEP intervention.
Abbreviations: ESAS-r, Edmonton Symptom Assessment System-revised; PC, palliative care; PCC, palliative care clinic; STEP, Symptom screening with Targeted Early Palliative care.
aGroup 1 symptoms: pain, dyspnea, nausea, depression, anxiety.
bGroup 2 symptoms: fatigue, drowsiness, appetite, well-being.
Citation: Journal of the National Comprehensive Cancer Network 20, 4; 10.6004/jnccn.2020.7803
STEP intervention.
Abbreviations: ESAS-r, Edmonton Symptom Assessment System-revised; PC, palliative care; PCC, palliative care clinic; STEP, Symptom screening with Targeted Early Palliative care.
aGroup 1 symptoms: pain, dyspnea, nausea, depression, anxiety.
bGroup 2 symptoms: fatigue, drowsiness, appetite, well-being.
Citation: Journal of the National Comprehensive Cancer Network 20, 4; 10.6004/jnccn.2020.7803
STEP intervention.
Abbreviations: ESAS-r, Edmonton Symptom Assessment System-revised; PC, palliative care; PCC, palliative care clinic; STEP, Symptom screening with Targeted Early Palliative care.
aGroup 1 symptoms: pain, dyspnea, nausea, depression, anxiety.
bGroup 2 symptoms: fatigue, drowsiness, appetite, well-being.
Citation: Journal of the National Comprehensive Cancer Network 20, 4; 10.6004/jnccn.2020.7803
The triage nurse informed the patient’s oncologist of each call and its outcome and kept a log of this information. For those who declined the EPC visit, reasons were recorded and symptom screening was continued, with the possibility of a future triggered call. Patients accepting EPC were assessed within 2 weeks in the palliative care clinic and received assessment and follow-up according to a standardized process that has been described in detail previously.5,38 Briefly, patients received a 60- to 90-minute consultation, followed by monthly follow-up (lasting ∼30 minutes) for 4 months, and at 6 months. The visits included evidence-based assessment and treatment by a palliative care physician and nurse for symptoms, psychological distress, social difficulties, and advance care planning. Other disciplines were involved as necessary. Initial visits were focused on coping, support, and symptom management; later visits focused on treatment decision-making and advance care planning.38 A nurse-led telephone triage line was available, with after-hours physician telephone support ensuring 24/7 coverage. If needed, patients were referred for home nursing care (in conjunction with clinic visits), transfer to a home palliative care physician (when the patient’s ECOG performance status was ≥3, or when requested), and admission to the Princess Margaret Palliative Care Unit for urgent symptom control and/or terminal care. After completion of the study, patients were offered continued follow-up in the palliative care clinic.
Data Collection and PROs
PROs were distributed in person or by mail and completed at baseline and at 2, 4, and 6 months. Participants who did not return an assessment within 2 weeks received a reminder telephone call; those who were not reached after 3 reminders were considered lost to follow-up. QoL was assessed using the Functional Assessment of Chronic Illness Therapy-Spiritual Well-Being scale (FACIT-Sp; primary outcome), the Functional Assessment of Cancer Therapy-General-7 (FACT-G7) scale, and the Quality of Life at the End of Life (QUAL-E) scale.39–42 Symptom control was assessed using a modified, validated version of the ESAS-r: the ESAS-r-CS, which includes the 9 original ESAS-r symptoms with additional symptoms of constipation and sleep (CS)43; all 11 items are summed for the ESAS-r-CS score. The Patient Health Questionnaire-9 (PHQ-9) is a widely used assessment tool for screening, diagnosing, and measuring depression,44 which incorporates DSM-IV depression diagnostic criteria and has been used in EPC trials.9 The FAMCARE-Patient-16 (FAMCARE-P16) scale measures satisfaction with information-giving, availability of care, psychological care, and physical patient care in outpatients with advanced cancer and is well validated.45,46
Trial Feasibility Criteria
The primary aim of this phase II trial was to determine the feasibility of implementing STEP in patients with advanced cancer. Specific feasibility criteria were as follows: accrual of ≥100 patients in 12 months, ≥70% of patients completed ESAS-r screening for at least 70% of visits, ≥60% of screen-positive patients met at least once with the EPC team, and ≥60% of participants completed measures at each endpoint. These criteria were based on previous successful phase II and III trials of EPC5,7,47,48 and distress screening,24 and on recruitment targets for a larger phase III trial of the STEP intervention.
Statistical Analyses
We hypothesized that screen-positive patients would have worse QoL and other PROs at baseline and at subsequent timepoints than those who remained screen-negative. We also hypothesized that screen-positive patients who received EPC would have improved QoL, symptom control, mood, and satisfaction with care compared with those who did not receive EPC, controlling for baseline PROs, age, sex, tumor site, and baseline ESAS-r Distress score. The target sample size was 100, based on our feasibility criteria for this 1-year study. We compared patient characteristics and PROs at baseline for screen-positive versus screen-negative patients, and for patients eventually receiving or not receiving EPC, using the Fisher exact or Mann-Whitney U test. Similarly, we compared the frequency and severity of individual ESAS-r screening symptoms for patients who attended or did not attend the targeted EPC visit.
We examined trends for change over time among 3 groups: screen-positive and received EPC, screen-positive and did not receive EPC, and consistently screen-negative. We tested differences in trends over time among screen-positive patients who did or did not receive EPC, using a linear mixed-effect model (which can handle intermittent missing values) with a random intercept term to account for individual differences at baseline. Furthermore, we adjusted P values to correct for multiple testing using a stepdown Bonferroni correction procedure and performed a sensitivity analysis using a Markov Chain Monte Carlo multiple imputation for missing values. All analyses were performed using SAS 9.4 (SAS Institute Inc).
Results
Patient Characteristics and Feasibility Results
From November 2016 to January 2018, 249 patients were eligible and 116 completed baseline measures (see supplemental eFigure 1, available with this article at JNCCN.org), of whom 110 were recruited in 2017. Of the 116 who completed baseline measures, 89 (77%) completed screening for ≥70% of visits; 70 (60%) were screen-positive at some point in the study and received a phone call from the palliative care nurse. There were no significant differences in demographic characteristics or anticancer treatments between those who screened positive during the study and those who never screened positive, nor between those receiving versus not receiving EPC (Table 1). All baseline PROs except FAMCARE-P16 were substantially worse among those who screened positive versus those who never screened positive. Among those who screened positive, the baseline ESAS-r Distress and ESAS-r-CS scores were worse among those who did versus did not receive EPC.
Demographic and Clinical Characteristics
Of those who screened positive, 74% (n=52) agreed to attend the palliative care clinic (45 after screening positive the first time, and 7 after the second time), 56% (n=39) attended the clinic at least once within the 6-month trial period (32 after screening positive the first time, and 7 after the second time), 4 additional patients who screened positive (6%) accepted a referral but received EPC after the end of the study, and 3 patients who screened negative attended the clinic upon referral by their oncologist. The most frequent reasons for declining EPC were: symptoms improved or adequately managed (n=9), feeling overburdened by appointments (n=7), and not interested/did not return nurse’s call (n=7). One participant died before accepting/declining EPC, and another recorded a screen-positive score but no alert was received. Measure completion among all 116 patients was 76% (n=88) at 2 months, 68% (n=79) at 4 months, and 63% (n=73) at 6 months.
Frequency and Severity of Symptoms Triggering a Nursing Call
For the 70 patients who were screen-positive, the median number of triggering symptoms per patient at the first triggered call was 1 (range, 1–7) for the 32 patients who attended the offered EPC visit and 2 (range, 1–9) for the 38 who did not attend. The mean severity of all triggering symptoms was 6.20 (SD, 1.87) for those who attended the EPC visit and 5.91 (SD, 1.52) for those who did not attend (P=.48). The means for individual triggering symptoms of patients who attended/did not attend the offered EPC visit are shown in Figure 2. The most common triggering symptoms were anxiety (n=33; 47%), pain (n=28; 40%), and depression (n=25; 36%). EPC attendance was highest for pain as a triggering symptom (16/28; 57%) and lowest for appetite (2/7; 29%).
Mean severity of symptoms for first triggered call among patients who did or did not attend the palliative care clinic visit. Symptoms were screened at outpatient oncology visits using the ESAS-r instrument and were rated from 0 to 10, where 0 indicated the absence of symptoms and 10 indicated the worst possible symptom severity.
Abbreviation: ESAS-r, Edmonton Symptom Assessment System-revised.
Citation: Journal of the National Comprehensive Cancer Network 20, 4; 10.6004/jnccn.2020.7803
Mean severity of symptoms for first triggered call among patients who did or did not attend the palliative care clinic visit. Symptoms were screened at outpatient oncology visits using the ESAS-r instrument and were rated from 0 to 10, where 0 indicated the absence of symptoms and 10 indicated the worst possible symptom severity.
Abbreviation: ESAS-r, Edmonton Symptom Assessment System-revised.
Citation: Journal of the National Comprehensive Cancer Network 20, 4; 10.6004/jnccn.2020.7803
Mean severity of symptoms for first triggered call among patients who did or did not attend the palliative care clinic visit. Symptoms were screened at outpatient oncology visits using the ESAS-r instrument and were rated from 0 to 10, where 0 indicated the absence of symptoms and 10 indicated the worst possible symptom severity.
Abbreviation: ESAS-r, Edmonton Symptom Assessment System-revised.
Citation: Journal of the National Comprehensive Cancer Network 20, 4; 10.6004/jnccn.2020.7803
For those who declined and received a second triggered call (n=12), the median number of triggering symptoms per patient at the second trigger was 2 (range, 2–5) for patients who attended the EPC visit versus 1 (range, 1–2) for patients who did not attend, and the mean of the triggering symptoms was 5.15 (SD, 1.52) for patients who attended versus 5.31 (SD, 1.25) for those who did not attend. Means for individual symptoms are shown in supplemental eFigure 2. The most common triggering symptoms for the second call were anxiety (n=9; 75%) and depression (n=5; 42%). In total, 11 patients ultimately attended 1 EPC visit, 7 attended 2 visits, and 21 attended ≥3 visits.
Trends Over Time According to Screening and Receipt of EPC
Figure 3 shows trends in the means for QoL (FACIT-Sp, FACT-G7, QUAL-E), symptom severity (ESAS-r-CS), depression (PHQ-9), and satisfaction with care (FAMCARE-P16), according to 3 patient groups: never screen-positive, screen-positive and received EPC, and screen-positive and did not receive EPC. Compared with those who screened positive, patients who never screened positive had substantially better QoL and other PROs at baseline, except satisfaction with care, which showed similar results; all PROs for those who never screened positive remained stable over the 6-month study period.
Patient-reported outcomes over time for patients who were screen-negative and for those who were screen-positive who either did or did not receive early palliative care (n=116). Higher scores are better for FACIT-Sp, FACT-G7, QUAL-E, and FAMCARE; higher scores are worse for ESAS-r-CS and PHQ-9.
Abbreviations: EPC, early palliative care; ESAS-r-CS, Edmonton Symptom Assessment System-revised, with the additional symptoms of constipation and sleep; FACIT-Sp, Functional Assessment of Chronic Illness Therapy-Spiritual Well-Being scale; FACT-G7, Functional Assessment of Cancer Therapy-General-7 scale; FAMCARE-P16, FAMCARE-Patient scale; PHQ-9, Patient Health Questionnaire-9; QUAL-E, Quality of Life at the End of Life scale.
Citation: Journal of the National Comprehensive Cancer Network 20, 4; 10.6004/jnccn.2020.7803
Patient-reported outcomes over time for patients who were screen-negative and for those who were screen-positive who either did or did not receive early palliative care (n=116). Higher scores are better for FACIT-Sp, FACT-G7, QUAL-E, and FAMCARE; higher scores are worse for ESAS-r-CS and PHQ-9.
Abbreviations: EPC, early palliative care; ESAS-r-CS, Edmonton Symptom Assessment System-revised, with the additional symptoms of constipation and sleep; FACIT-Sp, Functional Assessment of Chronic Illness Therapy-Spiritual Well-Being scale; FACT-G7, Functional Assessment of Cancer Therapy-General-7 scale; FAMCARE-P16, FAMCARE-Patient scale; PHQ-9, Patient Health Questionnaire-9; QUAL-E, Quality of Life at the End of Life scale.
Citation: Journal of the National Comprehensive Cancer Network 20, 4; 10.6004/jnccn.2020.7803
Patient-reported outcomes over time for patients who were screen-negative and for those who were screen-positive who either did or did not receive early palliative care (n=116). Higher scores are better for FACIT-Sp, FACT-G7, QUAL-E, and FAMCARE; higher scores are worse for ESAS-r-CS and PHQ-9.
Abbreviations: EPC, early palliative care; ESAS-r-CS, Edmonton Symptom Assessment System-revised, with the additional symptoms of constipation and sleep; FACIT-Sp, Functional Assessment of Chronic Illness Therapy-Spiritual Well-Being scale; FACT-G7, Functional Assessment of Cancer Therapy-General-7 scale; FAMCARE-P16, FAMCARE-Patient scale; PHQ-9, Patient Health Questionnaire-9; QUAL-E, Quality of Life at the End of Life scale.
Citation: Journal of the National Comprehensive Cancer Network 20, 4; 10.6004/jnccn.2020.7803
Among patients who screened positive, there were no significant differences in trends over time for those receiving versus those not receiving EPC in the FACIT-Sp, FACT-G7, QUAL-E, or FAMCARE-P16. However, there were significant differences in trends over time for the ESAS-r-CS and PHQ-9, which worsened among patients who did not receive EPC and improved among those who received EPC (Figure 3, supplemental eTable 1). These trends remained significant when adjusting for age, sex, tumor site, and baseline ESAS-r Distress score: for the ESAS-r-CS, the adjusted estimated change per month in those who received EPC versus those who did not receive EPC was –1.88 (SE, 0.63; P=.004 [P=.02 with Bonferroni correction]); for the PHQ-9 it was –0.57 (SE, 0.17; P=.001 [P=.006 with Bonferroni correction]) (supplemental eTable 1).
Discussion
This phase II trial showed the feasibility of STEP for patients with advanced cancer. Recruitment was successful, >75% completed symptom screening for at least 70% of clinic visits, and >60% completed measures at each timepoint. A total of 60% of participants screened positive; of these, 56% met at least once with the palliative care team during the trial and 6% were seen after the end of the study. Those who never screened positive had better PROs at baseline than those who screened positive, and they maintained these favorable outcomes over time. Among those who screened positive, those who received EPC had improved mood and improved symptom control over time, compared with those who did not receive EPC. These results are important in the planning of future trials and for clinical practice for patients with advanced cancer.
This trial shows that a subset of patients can be identified who will maintain good QoL, mood, symptom control, and satisfaction with care without early specialized palliative care intervention. For the 40% of patients in this study who never screened positive, QoL, symptoms, and mood were not only substantially better at baseline than for those who screened positive, but also remained stable over time. Previous trials have used a model in which EPC was provided routinely for all patients with advanced cancer.5–9 Our trial indicates that routine EPC may not be necessary for those with mild physical or psychological symptoms. In light of scarce resources and shortages of palliative care physicians worldwide,14,15 it may be most efficient to provide EPC only for those with moderate to severe symptoms according to specific screening criteria.
Patients who screened positive were given the option of booking an appointment for EPC or declining and continuing with symptom screening. Those who did not receive EPC tended to have less symptom distress at baseline than those who received EPC. However, even taking these baseline differences into account, patients who received EPC had improved mood and symptom control over time compared with those who did not receive EPC. A latent reason for declining may be stigma associated with palliative care and its association with the end of life.21 Further efforts are required to destigmatize palliative care and to develop user-friendly methods of access, such as virtual consultations.49,50
Anxiety, depression, and pain were the most common symptoms that triggered a nursing call and for which patients accepted EPC. Correspondingly, both mood and symptom control improved over time in those who received EPC compared with those who did not receive EPC. It may be possible to show improvements in QoL and satisfaction with care only with longer follow-up, even when using a targeted model of EPC delivery. Although symptom management and provision of psychological support are prominent goals of EPC during the initial palliative care consultation, later visits address advance care planning and treatment decisions.38,51 In previous studies, a higher proportion of EPC visits addressing coping was associated with both improved QoL and decreased depression,52 whereas a greater number of palliative care visits per month was associated with decreased aggressiveness of care, including less use of anticancer treatment at the end of life.53
Our study had limitations. Screening was performed only for physical and psychological symptoms, although patients may have had other social difficulties and unmet needs. Screening for these more complex needs is feasible,33 but our intent was to use a simple screening procedure that was already in practice and could quickly identify needs without undue burden. In addition, we screened only patients’ symptoms, whereas palliative care is aimed broadly at the patient and family, including family caregivers.54 Consistent with regional mandates,31 screening was performed only in the cancer center, before oncology visits; remote screening from home at regular intervals may have identified symptoms earlier, enabling more timely EPC intervention. Despite these limitations in screening, QoL and other PROs remained high for patients who never screened positive, indicating that this method of screening identified those for whom the impact on QoL was greatest. A larger proportion of patients than expected declined the targeted EPC visit, and outcomes for this group were worse than for those who received EPC. Although our analyses of these outcomes were adjusted for baseline ESAS-r Distress score, sex, and tumor site, there may have been other unmeasured variables that differed between the groups. To standardize the intervention, a trained palliative care nurse received the emails triggered by moderate to severe symptom scores and discussed EPC referral. Acceptance of EPC may have been increased if this discussion had been facilitated by a trusted oncology team member.
Conclusions
This phase II trial showed that patients with mild or no symptoms may not require EPC intervention to maintain good QoL. STEP identified those who were most likely to benefit from EPC and indicated improvements in those who attended the targeted EPC visit compared with those who declined EPC. Based on these findings, a multicenter randomized trial of STEP versus standard palliative care in patients with advanced cancer is underway.
Acknowledgments
The authors thank the patients who participated in this study, the medical oncologists who referred patients to this study, and the clinical and administrative staff of the palliative care team at the Princess Margaret Cancer Centre for their facilitation of this research, particularly Christine Cameron, RN. We also extend our thanks to Samantha Lo, clinical research study assistant, who assisted with the abstraction of data from the electronic patient record.
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