Abstract
Purpose:
We examined the change in outpatient PC services at US cancer centers over the past decade.
Methods:
Between April and August 2018, we surveyed all National Cancer Institute-designated cancer centers (NCI-CCs) and a random sample of 1252 non-NCI-CCs. Two surveys used previously in a 2009 national study (Hui et al. JAMA 2009) were sent to each institution: a 22-question cancer center executive survey regarding PC infrastructure and attitudes toward PC, and an 82-question PC program leader survey regarding detailed PC structures and processes. Survey findings from 2018 were compared to 2009 data from 101 cancer center executives and 96 PC program leaders.
Results:
The overall response rate was 140/203 (69%) for the cancer center executive survey and 123/164 (75%) for the PC program leader survey. Among NCI-CCs, a significant increase in outpatient PC clinics was observed between 2009 and 2018 (59% v. 95%; OR=12.3, 95% CI 3.2–48.2; P<.001) with no significant change in inpatient consultation teams (92% v. 90%; P=.71), PC units (26% v. 40%; P=.17), or institution-operated hospices (31% v. 18%; P=.14). Among non-NCI-CCs, there was no significant increase in outpatient PC clinics (22% v. 40%; P=.07), inpatient consultation teams (56% v. 68%; P=.27), PC units (20% v. 18%; P=.76) or institution-operated hospices (42% v. 23%; P=.05). The median interval from outpatient PC referral to death increased significantly, particularly for NCI-CCs (90 d v. 180 d; P=0.01).
Conclusions:
Despite significant growth in outpatient PC clinics, there remain opportunities for improvement in the structures and processes of PC programs.
Keywords: Health Services, Neoplasms, Outpatient Clinics, Hospital, Palliative Care, Surveys, Questionnaires
Precis:
In this national survey, the proportion of cancer centers with outpatient palliative care increased significantly between 2009 and 2018 among NCI-designated cancer centers (59% v. 95%) but not significantly at non-NCI designated cancer centers (22% v. 40%). Palliative care units remained uncommon and major gaps remain in palliative care clinical programs, particularly non-NCI designated cancer centers.
INTRODUCTION
Patients with advanced cancer often experience distressing symptoms and have significant supportive care needs along the disease trajectory.1 Many may benefit from specialist palliative care through outpatient clinics, inpatient consultation teams, palliative care units (PCUs) and community-based teams.2 Outpatient clinics are particularly well positioned to improve patient care outcomes by providing proactive symptom management, longitudinal psychosocial care, and advance care planning.3
In a 2009 national survey, 30/51 (59%) National Cancer Institute (NCI)-designated cancer centers, and 11/50 (22%) of non-NCI-designated cancer centers, reported having outpatient palliative care clinics.4 This survey was conducted prior to publication of multiple studies reporting that timely palliative care improves patients’ quality of life, symptom burden, quality of end-of-life care, satisfaction, communication, caregiver outcomes and cost of care.5–12 This body of knowledge has led to calls by several national organizations to involve specialist palliative care early in the disease trajectory for patients with advanced cancer, including the Institute of Medicine and the American Society for Clinical Oncology.13–15
The current landscape of palliative care services at US cancer centers is not fully known, with only a small survey in 2015 examining 22 centers within the National Comprehensive Cancer Network.16 A better understanding of the current level of palliative care availability nationwide could inform policy makers and hospital administrators in developing specific strategies to improve palliative care access. In this national survey, we aimed to obtain an updated estimate of the proportion of cancer centers with palliative care outpatient clinics, and to evaluate the change in this measure between 2009 and 2018. We hypothesized that the number of outpatient palliative care clinics has grown over the past decade. We also examined the structures and processes of outpatient clinics, inpatient consultation teams, PCUs and institution-operated hospices.
METHODS
Survey Development
This study included two separate surveys for each cancer center, one directed to the cancer center executive and the other to the palliative care program leader where applicable. These survey questions had been used in several national and international studies4, 17–20 and the methodology for survey creation had been reported previously.4 Briefly, 4 medical oncologists and 3 palliative care specialists generated the questions on the structures, processes and outcomes of specialist palliative care programs after conducting a comprehensive review of medical literature and National palliative care guidelines, with further pilot testing for readability and face validity. The cancer center executive survey included 22 questions to examine general access and attitudes toward palliative care (eAppendix 1). The palliative care program leader survey had 82 questions designed to assess details of program operations, including personnel, outpatient clinics, inpatient PCUs, consultation teams, hospice, and educational and research activities (eAppendix 2). To facilitate direct comparison against the 2009 findings, the same survey questions and answer options were used in 2018.4 The 2018 palliative care program leader survey also included eight new questions that assessed the level of integration of oncologic and palliative care within a given cancer center according to indicators developed by an international panel.20, 21 This study protocol was reviewed by the Institutional Review Board at The University of Texas MD Anderson Cancer Center and granted exemption status. This manuscript focuses on reporting the clinical structures and processes of palliative care services.
Cancer Centers
The surveys were sent to a sample of cancer centers accredited by the Commission of Cancer (CoC), a designation indicating the centers met 34 published standards.22 These centers represent approximately 30% of all US hospitals, and provide care to approximately 70% of patients with cancer.23, 24 Cancer centers demonstrating scientific excellence in cancer prevention, diagnosis, and treatment are separately recognized by NCI. NCI-designated cancer centers are generally large referral centers with access to greater resources. At the time of the survey, the CoC database included 62 NCI-designated cancer centers and 1252 non-NCI designated cancer centers.
The 2018 survey included four cohorts of cancer centers (Figure 1). The NCI-current cohort included all 62 existing NCI-designated cancer centers. The non-NCI-current cohort included a sample of 60 out of 1252 non-NCI-designated cancer centers selected using a simple randomization scheme; centers that were previously surveyed in 2009 were excluded from this cohort to ensure the 2009 and 2018 samples were independent. The NCI-previous cohort and the non-NCI-previous cohort included the same centers that were previously surveyed in 2009 (Figure 1). At the time of survey, 54 of 71 previously surveyed NCI-designated cancer centers and 66 of 71 non-NCI-designated cancer centers remained open while the others no longer exist. We defined a priori that data from the NCI-current and non-NCI-current cohorts constituted the main analyses. Data from the NCI-previous and non-NCI previous cohorts were complementary and shown in eTables 2–4.
Figure 1. Study Design: Sampling Strategy and Analysis Plan.
(A) In 2009, we surveyed all 71 National Cancer Institute (NCI)-designated cancer centers and a random sample of 71 non-NCI designated cancer centers. In 2018, some cancer centers had changed designation or no longer open and some centers newly acquired the Commission of Cancer or NCI-designation. Thus, we surveyed all 70 previously surveyed NCI-designated cancer centers in 2009 (NCI previous cohort) and all existing 62 NCI-designated cancer centers in 2018 (NCI current cohort). We also surveyed all 66 previously surveyed non-NCI-designated cancer centers in 2009 (non-NCI previous cohort) and a new sample of 60 non-NCI-designated cancer centers in 2018 (non-NCI current cohort). For NCI-current cohort, because there were only a limited number of NCI-designated cancer centers, we had to survey all of them and could not examine a new sample as in the case for non-NCI current cohort. (B) In main analysis, we compared 2009 cohorts to 2018 current cohorts. In secondary analysis, we compared 2009 cohorts to 2018 previous cohorts.
Survey Process
Similar to the previous study,4 contact information of cancer center executives and palliative care leaders were collected through the CoC, NCI, and institutional websites; this information was verified through independent telephone contact. All survey participants were mailed an invitation, a copy of the survey, and a $10 gift card without commitment to participate. Survey participants or their delegates were asked to complete the survey anonymously and to return it by mail, fax, or electronically through a secured website (www.qualtrics.com). Non-respondents were sent a reminder letter at 2 and 4 weeks, followed by phone or e-mail reminders after 8 weeks. Data collection occurred between April and August 2018.
Response Rate Calculation
Response rates were calculated according to the 2016 definitions published by the American Association for Public Opinion Research.25 Specifically, response rate was calculated as ((number of complete responses + number of partial responses)/(number of complete responses + number of partial responses + number of non-response + number of explicit refusals + number of implicit refusals)). In this study, a complete response was defined as completion of the key question (Question IIE for the cancer center executive survey and Question IE for the palliative care program leader survey) and ≥80% of questions. Partial response was defined as completion of the key question and <80% of questions. Non-response was defined as not answering the key question.
Statistical Analysis
The primary outcome was presence or absence of an outpatient palliative care clinic based on Question IIE for the cancer center executive survey. Assuming a response rate of 65%, we calculated that a sample size of 61 cancer centers would allow us to estimate the proportion of centers with an outpatient palliative care clinic with a standard error of ≤.079 for both NCI-designated and non-NCI-designated cancer centers.
The structures and processes of palliative care programs were reported and compared to 2009. Descriptive statistics such as proportion, 95% confidence interval (CI), mean, standard deviation (SD), median, and interquartile range (IQR) were used to summarize the extent of palliative care services in various cohorts. The Fisher’s exact test was used to examine the association between survey response and center type, and the association between center selection and state region distribution. To account for the partially overlapping data structure, generalized linear mixed model was used to examine the change in palliative care services between the 2009 NCI cohort and 2018 NCI-current cohort for both categorical and continuous variables. Logistic regression was used to examine the change between the 2009 non-NCI cohort vs. 2018 non-NCI-current cohort for categorical variables and the Wilcoxon rank sum test was used for continuous variables. Generalized linear mixed model was also used to examine changes between 2009 and 2018 previous cohorts. The primary outcome had no missing data and secondary outcomes were not imputed. Statistical testing was not conducted for variables in which the number of patients was too small (n<2) in some cells.
A P-value of <.05 was considered statistically significant for the primary outcome. For secondary outcomes, the focus was on estimates and 95% CIs; P-values were provided for hypothesis-generating purposes. The IBM SPSS Statistics for Windows, Version 24.0 (IBM Corp., Armonk, NY) and SAS 9.4 (SAS Institute Inc, Cary, NC) were used for statistical analyses.
RESULTS
Survey Response and Center Characteristics
The overall response rate was 140/203 (69%) for the cancer center executive survey and 123/164 (75%) for the palliative care program leader survey. Among NCI-designated cancer centers, 52/77 (68%) cancer center executives and 61/76 (80%) palliative care program leaders responded. Among non-NCI-designated cancer centers, 88/126 (70%) cancer center executives and 62/88 (71%) palliative care program leaders responded. The response rates for individual cohorts are shown in eTable 1.
There was no significant difference in state region distribution between non-NCI-designated cancer centers randomly selected for the survey (2018 non-NCI-current cohort) and those not sampled (P=.35). The overall response rate did not differ significantly between NCI and non-NCI-designated cancer centers (cancer center executive survey P=.87; palliative care program leader survey P=.21).
For the current cohorts, the median (IQR) number of inpatient beds was 100 (44–555) for NCI-designated cancer centers, and 25 (14–89) for non-NCI-designated cancer centers. The median (IQR) of outpatients was reported to be 5800 (700, 50,000) at NCI-designated cancer centers and 900 (105, 3,500) in non-NCI cancer centers.
Availability of Palliative Care Services: Current Cohorts
Figure 2 shows the availability of palliative care services according to the cancer center executive survey. Among NCI-designated cancer centers, there was a significant increase in outpatient clinics between 2009 and 2018 (59% v. 95%; OR 12.3, 95% CI 3.2–48.2; P<.001), but no significant change in inpatient consultation teams, PCUs or institution-operated hospices.
Figure 2. Changes in the Availability of Palliative Care Clinical Programs between 2009 and 2018.

Cancer center executives reported that there was a significant increase in the availability of outpatient clinics, although the other services including inpatient consultation teams, palliative care units and institutional-run hospices remained stagnant.
Among non-NCI-designated cancer centers, there was no statistically significant increase in outpatient clinics (22% v. 40%; OR 2.36, 95% CI 0.94, 5.94; P=.07) over the past decade. No significant change in inpatient consultation teams, PCUs, or institution-operated hospices was observed (Figure 2, Table 1).
Table 1.
Cancer Center Executive Survey: Palliative Care Structure
| NCI-Designated Cancer Centers | Non-NCI-Designated Cancer Centers | |||||||
|---|---|---|---|---|---|---|---|---|
| Characteristics | 2009 N=51 (%) [95% CI] | 2018 N=40 (%) [95% CI] | Odds Ratio (95% CI)a | P-valuea | 2009 N=50 (%) [95% CI] | 2018 N=40 (%) [95% CI] | Odds Ratio (95% CI)b | P-valueb |
| Palliative care available any time over the last 10 y | ||||||||
| Yes | 50 (98) [91.2, 99.8] | 40 (100) | - | - | 39 (78) [65.2, 87.7] | 35 (87.5) [74.8, 95.1] | 1.97 (0.62, 6.24) | 0.25 |
| No | 1 (2) [0.2, 8.8] | 0 | 11 (22) [12.3, 34.8] | 5 (12.5) [4.9, 25.2] | ||||
| Palliative care is currently active | ||||||||
| Yes | 50 (98) [91.2, 99.8] | 40 (100) | - | - | 39 (78) [65.2, 87.7] | 33 (82.5) [68.7, 91.8] | 1.33 (0.46, 3.82) | 0.60 |
| No | 1 (2) [0.2, 8.8] | 0 | 11 (22) [12.3, 34.8] | 7 (17.5) [8.2, 31.3] | ||||
| Palliative care structure | ||||||||
| Outpatient clinic | 30 (58.8) [45.1, 71.5] | 38 (95) [84.9, 98.9] | 12.33 (3.15, 48.18) | <.001 | 11 (22) [12.3, 34.8] | 16 (40) [25.9, 55.4] | 2.36 (0.94, 5.94) | 0.07 |
| Inpatient consultation team | 47 (92.2) [82.4, 97.3] | 36 (90) [78, 96.5] | 0.76 (0.18, 3.22) | 0.71 | 28 (56) [42.2, 69.1] | 27 (67.5) [52.2, 80.4] | 1.63 (0.69, 3.88) | 0.27 |
| Palliative care unit | 13 (25.5) [15.1, 38.6] | 16 (40) [25.9, 55.4] | 1.88 (0.76, 4.69) | 0.17 | 10 (20) [10.8, 32.6] | 7 (17.5) [8.2, 31.3] | 0.85 (0.29, 2.47) | 0.76 |
| Institution-operated hospice | 16 (31.4) [19.9, 44.9] | 7 (17.5) [8.2, 31.3] | 0.49 (0.18, 1.28) | 0.14 | 21 (42) [29.1, 55.8] | 9 (22.5) [11.8, 37.1] | 0.40 (0.16, 1.02) | 0.05 |
| Profession of palliative care program leaderc | ||||||||
| Physician | 43 (86) [74.5, 93.5] | 37 (92.5) [81.3, 97.8] | 1.66 (0.69, 4.01) | 0.26 | 30 (78.9) [64.2, 89.5] | 23 (69.7) [52.9, 83.2] | 0.61 (0.21, 1.80) | 0.37 |
| Advanced nurse practitioner | 4 (8) [2.8, 17.9] | 2 (5) [1.1, 15.1] | 2 (5.3) [1.1, 15.8] | 5 (15.2) [6, 30.1] | ||||
| Other | 3 (6) [1.7, 15.2] | 1 (2.5) [0.3, 11.1] | 6 (15.8) [6.9, 29.7] | 5 (15.2) [6, 30.1] | ||||
| Palliative care physician present | ||||||||
| Yes | 46 (92) [82.1, 97.2] | 39 (97.5) [88.9, 99.7] | 3.27 (0.36, 29.86) | 0.29 | 28 (73.7) [58.3, 85.6] | 26 (78.8) [62.8, 90] | 1.33 (0.44, 4.00) | 0.62 |
| No | 4 (8) [2.8, 17.9] | 1 (2.5) [0.3, 11.1] | 10 (26.3) [14.4, 41.7] | 7 (21.2) [10, 37.2] | ||||
Abbreviations: CI, confidence interval; IQR, interquartile range; NCI, National Cancer Institute; SD, standard deviation
Generalized linear mixed model was used to examine the change in each variable between 2009 NCI cohort and 2018 NCI-current cohorts
Logistic regression was used to examine the change in each variable between 2009 non-NCI cohort and 2018 non-NCI-current cohort
Odds ratio estimates reflect the proportion of centers reporting ‘Physician’ as palliative care program leader versus ‘advanced nurse practitioner’ and ‘Other’.
Palliative Care Service Structures and Processes: Current Cohorts
As shown in Table 2, palliative care program leaders reported that “palliative care” remains the most commonly used name for a majority of programs. The name “Supportive Care” was adopted by 18 (35%) NCI-designated cancer centers and 8 (30%) non-NCI-designated cancer centers. A smaller proportion of NCI-designated centers (50% vs. 31%, P=.002) and non-NCI-designated cancer centers (65% vs. 37%, P=.03) reported receiving referrals ≤4 weeks before death (Table 2).
Table 2.
Palliative Care Program Leader Survey: Clinical Program Overview
| NCI-Designated Cancer Centers | Non-NCI-Designated Cancer Centers | |||||||
|---|---|---|---|---|---|---|---|---|
| Characteristics | 2009 N=61 (%) [95% CI] | 2018 N=52 (%) [95% CI] | Odds Ratio (95% CI)a | P-valuea | 2009 N=35 (%) [95% CI] | 2018 N=27 (%) [95% CI] | Odds Ratio (95% CI)b | P-valueb |
| Name of palliative care program | ||||||||
| Comprehensive cancer care | 1 (1.7) [0.2, 7.5] | 5 (9.8) [3.8, 20.2] | - | - | 3 (8.6) [2.5, 21.1] | 0 | - | - |
| Pain and symptom management | 4 (6.7) [2.3, 15.1] | 0 | 6 (17.1) [7.5, 32] | 0 | ||||
| Palliative care | 43 (71.7) [59.4, 81.9] | 38 (74.5) [61.4, 84.9] | 28 (80) [64.7, 90.6] | 22 (81.5) [64.1, 92.6] | ||||
| Supportive care | 6 (10) [4.3, 19.5] | 18 (35.3) [23.3, 48.9] | 7 (20) [9.4, 35.3] | 8 (29.6) [15.1, 48.2] | ||||
| Other | 17 (28.3) [18.1, 40.6] | 4 (7.8) [2.7, 17.6] | 4 (11.4) [4, 24.9] | 2 (7.4) [1.6, 21.7] | ||||
| Duration of palliative care programc | ||||||||
| <1 y | 1 (1.7) [0.2, 7.8] | 3 (5.8) [1.7, 14.6] | 5.96 (2.35, 15.10) | <.001 | 4 (12.1) [4.2, 26.3] | 3 (11.5) [3.4, 27.7] | 5.04 (1.65, 15.34) | 0.004 |
| 1–2 y | 13 (22.4) [13.2, 34.3] | 0 | 5 (15.2) [6, 30.1] | 2 (7.7) [1.6, 22.5] | ||||
| 3–5 y | 14 (24.1) [14.6, 36.2] | 4 (7.7) [2.7, 17.3] | 15 (45.5) [29.4, 62.2] | 4 (15.4) [5.4, 32.5] | ||||
| >5 y | 30 (51.7) [39, 64.2] | 45 (86.5) [75.4, 93.8] | 9 (27.3) [14.4, 43.9] | 17 (65.4) [46.3, 81.3] | ||||
| Palliative care structure | ||||||||
| Outpatient clinic | 40 (66.7) [54.2, 77.6] | 51 (98.1) [91.4, 99.8] | 24.52 (3.51, 171.44) | 0.001 | 10 (28.6) [15.7, 44.8] | 17 (63) [44.2, 79.1] | 4.25 (1.46, 12.41) | 0.008 |
| Inpatient consultation team | 53 (88.3) [78.5, 94.6] | 50 (96.2) [88.2, 99.2] | 3.31 (0.66, 16.54) | 0.15 | 29 (82.9) [68, 92.5] | 24 (88.9) [73.2, 96.8] | 1.66 (0.37, 7.33) | 0.51 |
| Palliative care unit | 16 (26.7) [16.8, 38.8] | 15 (28.8) [17.9, 42.1] | 0.91 (0.41, 2.02) | 0.83 | 11 (31.4) [18, 47.8] | 3 (11.1) [3.2, 26.8] | 0.27 (0.07, 1.10) | 0.07 |
| Institution-operated hospice | 17 (28.3) [18.1, 40.6] | 13 (25) [14.8, 37.9] | 0.99 (0.45, 2.18) | 0.98 | 24 (68.6) [52.2, 82] | 14 (51.9) [33.6, 69.7] | 0.49 (0.17, 1.39) | 0.18 |
| Palliative care team services offered | ||||||||
| Assessment and management of psychiatric disorders | 29 (47.5) [35.4, 59.9] | 33 (63.5) [49.9, 75.5] | 1.89 (0.90, 3.98) | 0.09 | 11 (31.4) [18, 47.8] | 7 (25.9) [12.4, 44.3] | 0.76 (0.25, 2.34) | 0.64 |
| Obtaining advance directives/DNR ordersd | 54 (88.5) [78.8, 94.7] | 51 (98.1) [91.4, 99.8] | 6.61 (0.79, 55.34) | 0.08 | 29 (82.9) [68, 92.5] | 26 (96.3) [84, 99.6] | 3.89 (0.59, 25.60) | 0.16 |
| Ethical issues | 44 (72.1) [60, 82.2] | 39 (75) [62.1, 85.2] | 1.16 (0.53, 2.57) | 0.71 | 29 (82.9) [68, 92.5] | 23 (85.2) [68.5, 94.8] | 1.19 (0.30, 4.72) | 0.80 |
| Referrals to hospice, home care, and other placements | 54 (88.5) [78.8, 94.7] | 49 (94.2) [85.4, 98.3] | 1.96 (0.57, 6.78) | 0.29 | 30 (85.7) [71.5, 94.3] | 25 (92.6) [78.3, 98.4] | 2.08 (0.37, 11.68) | 0.40 |
| Comprehensive care plan for those requiring comfort cared | 52 (85.2) [74.8, 92.4] | 48 (92.3) [82.7, 97.3] | 1.98 (0.60, 6.47) | 0.26 | 27 (77.1) [61.5, 88.6] | 26 (96.3) [84, 99.6] | 5.46 (0.86, 34.65) | 0.07 |
| Pain consultation | 56 (91.8) [83, 96.8] | 50 (96.2) [88.2, 99.2] | 2.25 (0.41, 12.43) | 0.35 | 31 (88.6) [75.1, 96] | 24 (88.9) [73.2, 96.8] | 1.03 (0.21, 5.06) | 0.97 |
| Psychosocial supportd | 53 (86.9) [76.8, 93.6] | 49 (94.2) [85.4, 98.3] | 2.44 (0.60, 9.97) | 0.22 | 25 (71.4) [55.2, 84.3] | 26 (96.3) [84, 99.6] | 7.28 (1.17, 45.22) | 0.03 |
| Symptom managementd | 56 (91.8) [83, 96.8] | 52 (100) | - | - | 33 (94.3) [82.9, 98.8] | 26 (96.3) [84, 99.6] | 1.32 (0.16, 11.01) | 0.80 |
| Proportion of patients in pediatric group (<18y)e | ||||||||
| 0% | 33 (54.1) [41.6, 66.2] | 25 (48.1) [34.9, 61.5] | 1.30 (0.71, 2.41) | 0.40 | 24 (68.6) [52.2, 82] | 20 (74.1) [55.7, 87.6] | 0.93 (0.29, 2.95) | 0.91 |
| 1–25% | 24 (39.3) [27.8, 51.9] | 26 (50) [36.7, 63.3] | 8 (22.9) [11.4, 38.5] | 7 (25.9) [12.4, 44.3] | ||||
| 26–50% | 0 | 0 | 0 | 0 | ||||
| 51–75% | 0 | 0 | 0 | 0 | ||||
| 76–100% | 1 (1.6) [0.2, 7.4] | 1 (1.9) [0.2, 8.6] | 1 (2.9) [0.3, 12.6] | 0 | ||||
| Estimated patient follow-up timef | ||||||||
| 1–7 d | 18 (31.6) [20.7, 44.3] | 0 | 3.21 (1.52, 6.81) | 0.002 | 13 (40.6) [25, 57.8] | 8 (29.6) [15.1, 48.2] | 3.25 (1.11, 9.45) | 0.03 |
| 1–4 wk | 16 (28.1) [17.7, 40.6] | 15 (31.3) [19.5, 45.2] | 8 (25) [12.6, 41.7] | 2 (7.4) [1.6, 21.7] | ||||
| 1–12 mo | 17 (29.8) [19.2, 42.5] | 21 (43.8) [30.4, 57.8] | 9 (28.1) [14.9, 45.1] | 14 (51.9) [33.6, 69.7] | ||||
| 1–2 y | 3 (5.3) [1.5, 13.4] | 9 (18.8) [9.7, 31.4] | 2 (6.3) [1.3, 18.6] | 1 (3.7) [0.4, 16] | ||||
| >2 y | 3 (5.3) [1.5, 13.4] | 3 (6.3) [1.8, 15.7] | 0 | 2 (7.4) [1.6, 21.7] | ||||
Abbreviations: CI, confidence interval; DNR, do not resuscitate; NCI, National Cancer Institute
Generalized linear mixed model was used to examine the change in each variable between 2009 NCI cohort and 2018 NCI-current cohorts.
Logistic regression was used to examine the change in each variable between 2009 non-NCI cohort and 2018 non-NCI-current cohort, unless otherwise specified.
Odds ratio estimates reflect the proportion of centers reporting ‘>5 years’ versus ‘≤5 years’.
Penalized logistic regression was fitted to adjust for categories with low frequency.
Odds ratio estimates reflect the proportion of centers reporting >0% versus 0%.
Odds ratio estimates reflect the proportion of centers reporting ‘> 1 month’ versus ‘≤ 1 month’.
Palliative care program leaders reported a significant improvement in the structures and processes for outpatient clinics (Table 3). Specifically, the number of stand-alone clinics (P=.002) and clinic day availability (P=.002) all increased significantly for NCI-designated cancer centers between 2009 and 2018. The median (IQR) interval from outpatient referral to death increased from 90 days (84, 120 days) to 180 days (131, 220 days) for NCI-designated cancer centers and from 41 days (28, 54 days) to 84 days (48, 120 days) for non-NCI-designated cancer centers (Table 3).
Table 3.
Palliative Care Program Leader Survey: Structures and Processes of Outpatient Clinics, Inpatient Consultation Teams, Palliative Care Units, and Institution-Operated Hospices
| NCI-Designated Cancer Centers | Non-NCI-Designated Cancer Centers | |||||||
|---|---|---|---|---|---|---|---|---|
| Characteristics | 2009 N=61 (%) [95% CI] | 2018 N=52 (%) [95% CI] | Odds Ratio (95% CI)a | P-valuea | 2009 N=35 (%) [95% CI] | 2018 N=27 (%) [95% CI] | Odds Ratio (95% CI)b | P-valueb |
| Outpatient clinics | ||||||||
| Dedicated (stand alone) outpatient clinics | 33 (55) [42.4, 67.1] | 43 (82.7) [70.8, 91.1] | 3.68 (1.60, 8.43) | 0.002 | 7 (20) [9.4, 35.3] | 11 (40.7) [23.9, 59.4] | 2.75 (0.89, 8.51) | 0.08 |
| Embedded in oncology clinics | 14 (23.3) [14, 35.1] | 20 (38.5) [26.2, 52] | 2.08 (0.93, 4.63) | 0.07 | 4 (11.4) [4, 24.9] | 8 (29.6) [15.1, 48.2] | 3.26 (0.86, 12.33) | 0.08 |
| No outpatient clinics | 20 (33.3) [22.4, 45.8] | 1 (1.9) [0.2, 8.6] | - | - | 25 (71.4) [55.2, 84.3] | 10 (37) [20.9, 55.8] | - | - |
| Number of clinic d/wk | ||||||||
| Mean (SD)c | 2.5 (2.0) | 4.4 (3.3) | 1.87 (0.69, 3.05) | 0.002 | 2.0 (2.0) | 2.8 (1.8) | 0.83 (−0.88, 2.55) | 0.22 |
| Median (IQR) | 2.0 [1.0, 4.5] | 5.0 [3.0, 5.0] | 1.0 [0.5, 3.5] | 3.0 [1.0, 5.0] | ||||
| Number of referrals/mo | ||||||||
| Mean (SD)c | 26.1 (44.2) | 35.2 (26.6) | 9.04 (−6.63, 24.70) | 0.25 | 10.1 (10.0) | 23.4 (25.7) | 13.27 (−2.11, 28.65) | 0.11 |
| Median (IQR) | 14.0 [6.0, 22.5] | 30.0 [17.5, 45.0] | 7.5 [2.0, 18.0] | 14.0 [8.0, 30.0] | ||||
| Days from referral to death | ||||||||
| Mean (SD) | 98.3 (55.8) | 192.7 (90.9) | 94.4 (23.1, 165.6) | 0.01 | 41 (18.4) | 83.8 (51.3) | - | - |
| Median (IQR) | 90 [84, 120] | 180 [131, 220] | 41 [28, 54] | 83.8 [47.5, 120] | ||||
| Inpatient consultation team | ||||||||
| Dedicated consultation service | 53 (88.3) [78.5, 94.6] | 50 (96.2) [88.2, 99.2] | 3.31 (0.66, 16.54) | 0.15 | 29 (82.9) [68, 92.5] | 24 (88.9) [73.2, 96.8] | 1.66 (0.37, 7.33) | 0.51 |
| Availabilityf | ||||||||
| 24 h/d, 7d/wk | 23 (46) [32.7, 59.7] | 31 (63.3) [49.3, 75.7] | 2.02 (0.98, 4.16) | 0.06 | 11 (37.9) [22.1, 56] | 8 (33.3) [17.2, 53.2] | 0.82 (0.26, 2.54) | 0.73 |
| 24 h/d, weekdays only | 3 (6) [1.7, 15.2] | 3 (6.1) [1.8, 15.4] | 1 (3.4) [0.4, 15] | 0 | ||||
| Business h, weekdays only | 22 (44) [30.9, 57.8] | 12 (24.5) [14.1, 37.8] | 13 (44.8) [27.9, 62.7] | 15 (62.5) [42.6, 79.6] | ||||
| Other | 2 (4) [0.8, 12.2] | 3 (6.1) [1.8, 15.4] | 4 (13.8) [4.8, 29.5] | 1 (4.2) [0.5, 17.9] | ||||
| Consultation serviceg | ||||||||
| 5 d/w | 26 (52) [38.4, 65.4] | 15 (30.6) [19.1, 44.3] | 2.26 (1.05, 4.84) | 0.04 | 15 (53.6) [35.5, 70.9] | 15 (62.5) [42.6, 79.6] | 0.69 (0.23, 2.10) | 0.52 |
| 6 d/w | 0 | 1 (2) [0.2, 9.1] | 0 | 0 | ||||
| 7 d/w | 24 (48) [34.6, 61.6] | 33 (67.3) [53.5, 79.2] | 13 (46.4) [29.1, 64.5] | 9 (37.5) [20.4, 57.4] | ||||
| Referrals/m | ||||||||
| Mean (SD) | 57.0 (40.1) | 117.1 (86.9) | - | - | 41.7 (41.3) | 87 (81) | - | - |
| Median (IQR) | 50.0 [30.0, 75.0] | 100.0 [70.0, 125.0] | 30 [19, 50] | 57.5 [40, 100] | ||||
| Days from referral to death | ||||||||
| Mean (SD) | 25.3 (47.8) | 49.6 (72.7) | - | - | 17.9 (28.1) | 31.9 (43.2) | - | - |
| Median (IQR) | 7.0 [4.0, 17.5] | 10.0 [7.0, 90.0] | 7 [4, 10] | 30 [4, 30] | ||||
| Inpatient palliative care units/beds | ||||||||
| Dedicated acute care beds (non-hospice) | 16 (26.7) [16.8, 38.8] | 15 (28.8) [17.9, 42.1] | 0.91 (0.41, 2.02) | 0.83 | 11 (31.4) [18.0, 47.8] | 3 (11.1) [3.2, 26.8] | 0.27 (0.07, 1.10) | 0.07 |
| Number of beds, mean (SD) | 10.2 (7.5) | 8.6 (5.0) | - | - | 5 (2) | 19 (0) | - | - |
| Median (IQR) | 10.5 [4.0, 12.0] | 10.0 [3.0, 12.0] | 4 [4, 6] | 19 [19, 19] | ||||
| Physical unit presente | 9 (69.2) [42.3, 88.6] | 13 (86.7) [63.7, 97.1] | 2.94 (0.51, 17.12) | 0.23 | 4 (40) [15.3, 69.6] | 1 (33.3) [3.9, 82.3] | 0.87 (0.06, 12.34) | 0.92 |
| Discharges/mo, median (IQR) | 45.0 [30.0, 50.0] | 30.0 [20.0, 36.0] | 15 [11.5, 26.5] | 34 [8, 60] | ||||
| Inpatient palliative care stays in days, median (IQR) | 6.0 [4.0, 9.0] | 5.0 [5.0, 7.0] | 4 [2.5, 6.9] | 5 [4, 7] | ||||
| Days from admission to death, median (IQR) | 6.0 [3.0, 21.0] | 4.5 [2.0, 10.0] | 7 [6.3, 7] | 4.5 [4.5, 4.5] | ||||
| PCU mortality rate, median (IQR) | 40.0 [28.0, 65.0] | 50.0 [46.0, 72.0] | 43 [25, 70] | 25 [0, 60] | ||||
| Unknown or not answered | 45 (73.8%) | 38 (73.1%) | 25 (71.4%) | 24 (88.9%) | ||||
| Institution-operated hospices | ||||||||
| In operation | 17 (28.3) [18.1, 40.6] | 13 (25) [14.8, 37.9] | 0.99 (0.45, 2.18) | 0.98 | 24 (68.6) [52.2, 82] | 14 (51.9) [33.6, 69.7] | 0.49 (0.17, 1.39) | 0.18 |
| Daily census, median (IQR) | 15 [7, 43] | 56.5 [25, 100] | 85 [19.5, 268] | 47.5 [22.5, 345] | ||||
Abbreviations: CI, confidence interval; IQR, interquartile range; NCI, National Cancer Institute; SD, standard deviation
Generalized linear mixed model was used to examine the change in each variable between 2009 NCI cohort and 2018 NCI-current cohorts, unless otherwise specified.
Logistic regression was used to examine the change in each variable between 2009 non-NCI cohort and 2018 non-NCI-current cohort, unless otherwise specified.
Mean difference (95% CI) is shown instead of odds ratio. P-value was computed with Wilcoxon rank sum test for non-NCI cancer centers.
P-value was computed with Fisher’s exact test for variables with small numbers in some cells for non-NCI cancer centers.
Penalized logistic regression was fitted to adjust for categories with low frequency.
Odds ratio estimates reflect the proportion of centers reporting ‘24 hours 7 days per week’ versus the rest.
Odds ratio estimates reflect the probability of ‘7d/w’ vs ‘5 or 6 d/w’ for “2018 NCI Current” versus “2009 NCI” or “2018 non-NCI Current” versus “2009 non-NCI”.
With few minor exceptions, there were no significant changes in the structures or processes of PCUs and inpatient consultation teams at NCI-designated and non-NCI-designated cancer centers.
Previous Cohorts Data
Data from centers that were previously surveyed in 2009 (i.e. previous cohorts) are shown in eTables 2–4. Among the NCI-designated cancer centers that responded, 37 cancer center executive surveys and 45 palliative care program leader surveys in the 2018 NCI-previous cohorts were the same as 2018 NCI-current cohorts. The primary outcome analysis in previous cohorts showed similar trends as the current cohorts (eTable 2). The findings from previous cohorts were similar to current cohorts (generally ±10%).
DISCUSSION
Compared to a decade ago, there has been an increase in outpatient palliative care services and educational programs at cancer centers. However, this expansion has been heterogeneous and mostly concentrated at NCI-designated cancer centers. The growth in inpatient PCUs remain stagnant. This survey highlights significant gaps in the delivery of palliative cancer care and opportunities for improvement.
Consistent with our hypothesis, there was a significant increase in outpatient palliative care services between 2009 and 2018. This growth is encouraging given that outpatient clinics represent the only branch of palliative care to facilitate timely referral in the ambulatory setting, and earlier referral to palliative care is associated with improved patient and caregiver outcomes.5, 6, 11 NCI-designated cancer centers reported that 95% of them were equipped with outpatient PC clinics, which is higher than previous national and international surveys.4, 16–20 However, this was true for less than half of non-NCI-designated cancer centers, which serve a large proportion of cancer patients in the US. The 2016 CoC Cancer Program Standard 2.4 mandates that “palliative care services are available to patients either on-site or by referral”;22 a more stringent requirement for outpatient palliative care clinics to be available on-site could significantly improve timely palliative care access.
The availability of palliative care services was assessed in both the cancer center executive survey and palliative care program leader survey. Differences in availability of services between these surveys was because we could only survey palliative care program leaders when a palliative care program was available while we surveyed cancer center executives at all cancer centers. As defined a priori, our primary outcome (i.e. outpatient clinic) was based on the cancer center executive survey instead of the palliative care program leader survey. Furthermore, not all cancer centers responded to both the cancer center executive and palliative care program leader surveys, resulting in different denominators. Despite these differences, we observed a significant increase in outpatient clinics in both surveys, suggesting our findings were robust.
The timing of referral remains an area for further improvement. Although the optimal timing of outpatient referral remains a subject of debate, an international consensus panel recommended a time frame of at least 6 months before death.26 Standardized criteria, coupled with systematic distress screening and automatic referral, may facilitate timely access to palliative care for more patients.26, 27 In our survey, the program name “Supportive Care” was used in approximately one third of cancer centers. Previous studies have reported that both patients and oncologists were much more willing to refer patients to palliative care earlier in the disease trajectory if ”Supportive Care” was used instead of “Palliative Care”.28–31
Another area of concern is that only a minority of NCI-designated and non-NCI-designated cancer centers reported having PCUs. Similar to the concept of intensive care units, PCUs are staffed by a highly specialized interdisciplinary team and typically reserved for patients who require intensive symptom management.32–34 In a study of bereaved caregivers, patients who died in PCUs were perceived to have better quality of end-of-life care than patients who died outside of PCUs.35 In the last weeks and days of life, symptoms such as dyspnea and agitated delirium become more prevalent and can be highly distressing.36, 37 The paucity of PCUs means that cancer patients suffering from severe distress in the last days of life may not have access to the most comprehensive form of end-of-life care. Furthermore, PCUs have an important role in conducting research to advance care in the last days of life; their relative absence significantly impedes scientific progress in this area.38–40
This study has several limitations. First, this survey was based on self-reported information and we did not independently verify the data. For some continuous variables (e.g. timing of referral), we asked respondents to provide approximations which may limit the accuracy with the potential for bias towards more favorable reporting. However, a majority of variables in this survey were binary in nature and thus did not require approximations. The surveys were addressed to cancer center executives and palliative care program leaders, although delegates were allowed to complete the surveys on their behalf. Second, non-NCI cancer centers were randomly selected from the CoC database, which mandated that palliative care services be available to patients either on-site or by referral since 2012.22 Thus, this group of centers may have a greater palliative care availability than non-CoC accredited centers. Third, only a small number of non-NCI cancer centers were sampled; however, this estimate was supplemented with a separate cohort of centers surveyed in 2009 and the findings were consistent. Fourth, approximately 50% of NCI designated cancer centers and 25% of non-NCI designated cancer centers reported providing services to pediatric patients. However, our study did not make a clear distinction between adult and pediatric services. Further research is needed to examine pediatric program operations. Fifth, this study focused on specialist palliative care and palliative care program leaders answered a majority of the questions about the program details. However, some respondents might have included primary palliative care in their responses. Sixth, we conducted statistical testing to examine changes between 2009 and 2018 on multiple secondary outcomes. Although a higher threshold was applied for statistical significance, the findings should be interpreted with caution and considered as hypothesis generating.
In summary, this survey documents slow progress in the growth of palliative care programs and highlights that access to timely palliative care remains a challenge for cancer patients, particularly those at non-NCI cancer centers. Data from this survey may help national health organizations to formulate policies, hospital administrators to benchmark their programs and allocate appropriate resources, and oncology and palliative care teams to develop quality improvement projects. With greater resources to support clinical programs, education, and research, we hope to achieve The American Society of Clinical Oncology’s vision towards full integration of palliative care as a routine part of comprehensive cancer care.15
Supplementary Material
Acknowledgements:
We are grateful to all respondents for completing the surveys. We would also like to thank Jane Naberhuis, PhD for assistance with table preparations.
Funding: This research was supported in part by a National Institutes of Health Cancer Center Support Grant (P30CA016672). Dr. Hui reported receiving grants from the National Institutes of Health (NIH)/National Cancer Institute (1R01CA214960-01A1; 1R01CA225701-01A1) and National Institute of Nursing Research (1R21NR016736-01), Helsinn Therapeutics and Insys Therapeutics during the conduct of the study. Dr. Delgado reported receiving a grant from NIH/NCI (R01CA200867). Dr. Bruera reported receiving grants from the NIH/NCI, NINR and Helsinn Therapeutics during the conduct of the study.
Footnotes
Conflict of interest: The authors declare no conflict of interest. The funding organizations had no role in the design or conduct of the study; in collection, management, analysis, or interpretation of the data; or in preparation, review, or approval of the manuscript.
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