Neuro-Oncology Practice
Neuro-Oncology Practice 2(2), 62 – 69, 2015
doi:10.1093/nop/npu037
Advance Access date 16 February 2015
International patterns of palliative care in neuro-oncology: a survey of
physician members of the Asian Society for Neuro-Oncology,
the European Association of Neuro-Oncology, and the Society
for Neuro-Oncology
Tobias Walbert, Vinay K. Puduvalli, Martin J.B. Taphoorn, Andrew R. Taylor, and Rakesh Jalali
Departments of Neurosurgery and Neurology, Henry Ford Health System, Detroit, Michigan (T.W., A.R.T.); The Ohio State University
Comprehensive Cancer Center, Columbus, Ohio (V.K.P.); VU University Medical Center, Amsterdam, Netherlands (M.J.B.T.); Medical Center
Haaglanden, The Hague, Netherlands (M.J.B.T.); Tata Memorial Centre, Mumbai, India (R.J.)
Corresponding Author: Tobias Walbert, MD, MPH, Departments of Neurosurgery and Neurology, Henry Ford Health System, 2799 W Grand Blvd, Detroit,
MI 48202 ([email protected]).
Background. Brain tumor patients have limited survival and suffer from high morbidity requiring specific symptom management.
Specialized palliative care (PC) services have been developed to address these symptoms and provide end-of-life treatment. Global
utilization patterns of PC in neuro-oncology are unknown.
Methods. In a collaborative effort between the Society for Neuro-Oncology (SNO), the European Association of Neuro-Oncology
(EANO), and the Asian Society for Neuro-Oncology (ASNO), a 22-question survey was distributed. Wilcoxon 2-sample and KruskalWallis tests were used to assess differences in responses.
Results. Five hundred fifty-two evaluable responses were received. The most significant differences were found between Asia-Oceania
(AO) and Europe as well as AO and United States/Canada (USA-C). USA-C providers had more subspecialty training in neuro-oncology,
but most providers had received no or minimal training in palliative care independent of region. Providers in all 3 regions reported
referring patients at the onset of symptoms requiring palliation, but USA-C and European responders refer a larger total proportion
of patients to PC (P , .001). Physicians in AO and Europe (both 46%) as well as 29% of USA-C providers did not feel comfortable dealing
with end-of-life issues. Most USA-C patients (63%) are referred to hospice compared with only 8% and 19% in AO and Europe (P ,
.001), respectively.
Conclusion. This is the first report describing global differences of PC utilization in neuro-oncology. Significant differences in provider
training, culture, access, and utilization were mainly found between AO and USA-C or AO and Europe. PC patterns are more similar in
Europe and USA-C.
Keywords: end-of-life, glioma, glioblastoma, hospice, palliative care.
Introduction
The most common primary brain tumors in adults are malignant
gliomas. These highly aggressive tumors are routinely treated
with maximal safe resection, followed by radiotherapy alone or
with concurrent and adjuvant chemotherapy to the residual
tumor and the surrounding brain tissue.1,2 Despite this aggressive
approach, the median survival for malignant gliomas is estimated
to be 2 – 5 years and 15 months for patients with glioblastoma.1,3,4 Recent gains in our understanding of the molecular differences among tumor types has facilitated the development of
novel therapies, but long-term survival still remains elusive for
most patients with malignant glioma. In the setting of limited
long-term survival, controlling symptoms and maintaining quality of life have become increasingly important goals.
Because palliative care (PC) might be defined differently in various regions, for our survey we used the World Health Organization’s definition that describes PC as a systematic and proactive
approach to managing issues that are important to patients
and families affected by serious illness.5 While it is the primary
goal of neuro-oncologists to treat the brain tumor and to extend
survival, PC focuses on patient well-being and symptom control,
which are equally important for this patient group. PC services are
provided by a multidisciplinary specialized team of physicians and
Received 9 October 2014; accepted 1 December 2014, Advance Access publication 16 February 2015
# The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Neuro-Oncology. All rights reserved.
For permissions, please e-mail: [email protected].
62
Walbert et al.: International patterns of palliative care in neuro-oncology
health care providers and can be utilized at any point along the
disease trajectory. PC is frequently misunderstood as being synonymous with end-of-life care. Therefore, it is important to understand that PC focuses on symptom management and can be part
of any treatment with curative intent.6 Concurrent PC has been
shown to improve quality of life in metastatic lung cancer patients and even prolong survival in these patients when utilized
early and in a systematic fashion.7 PC must be differentiated
from hospice care. Hospice care uses a similar approach, but is focused on controlling the pain and symptoms of patients with a
terminal diagnosis who are approaching end of life.8
Based on the positive findings of concurrent PC in metastatic
lung cancer, the American Society of Clinical Oncology has endorsed the integration of PC services into standard oncology
care at the time a patient is diagnosed with metastatic or advanced cancer.9 To our knowledge, no such formalized recommendations have been made in Asia or Europe.10 End-of-life
symptoms in high-grade glioma patients11,12 have been recently
reviewed, and it was found that brain tumor patients have a high
symptom burden and are frequently unable to make decisions
during the last weeks of life. Based on these findings, it has
been proposed that early involvement of PC in neuro-oncology12
might benefit the quality of life for patients as well as their caregivers. However, up to now the specific utilization patterns of PC
and hospice in the neuro-oncology community have been unknown. The goal of this international multisociety survey was to
determine the global pattern of PC utilization in neuro-oncology.
Methods
The instrument used for this study was an ad hoc survey questionnaire to assess the utilization patterns of PC and hospice in
the neuro-oncology community. The questionnaire was designed
by the investigators after extensive discussion and a comprehensive literature review of supportive care needs 13 and
end-of-life symptom management12 for brain tumor patients.
Special attention was given to the perception of PC in the oncology community.14,15
The questions were piloted internally and among the authors
and an external specialist in the field of PC. After review and modification by the authors, a final 22-question survey was agreed
upon (Table 1). Questions assessed demographics of the respondents (ie, age, sex, number of years in practice, practice setting,
number of brain tumor patients treated, subspecialty, and formal
training in palliative care as well as neuro-oncology) and specific
questions to assess the individual as well as the institutional approach toward PC and hospice. Institutional review board approval was secured at 3 sites internationally.
In a collaborative effort of the Society for Neuro-Oncology
(SNO), the European Association of Neuro-Oncology (EANO),
and the Asian Society for Neuro-Oncology (ASNO), the questionnaire was distributed to members of all 3 societies and participants at the annual SNO meeting in 2012 and the annual ASNO
meeting in 2013. All 3 surveys were in English-language format
and contained the same 22 questions and scales. The SNO and
the ASNO surveys were distributed electronically utilizing an online survey site (www.surveymonkey.com). A single electronic invitation was sent to everyone who submitted an abstract to the
2012 SNO meeting (n, 5400) and all participants of the 2013
Neuro-Oncology Practice
ASNO meeting (n, 1638). An additional paper copy was distributed at the SNO meeting quality-of-life session and the ASNO
meeting.
The EANO survey was sent electronically to all EANO members
(n, 752), and responses were returned via e-mail or fax. Because
we could not prevent participants from receiving more than one
invitation to complete the survey, all respondents were explicitly
asked to complete the survey only once. Only physician responses
(MD, DO, MD PhD, or fellow/resident) are reported in this article.
No incentives were offered for answering the survey. Physicians
who were not practicing in one of the 3 regions or who reported
a practice location of “other” and whose location could not be
identified by their Internet Protocol address were excluded from
the analyses. Practice setting was categorized as “Academic” (ie,
National Cancer Institutes designated, nondesignated academic,
government hospital, academic institution) or “All Other Hospitals” (nonacademic hospital-based, mission/trust hospital, independent practice, group practice, or solo practice).
Statistical Analysis
Demographic differences in responses to the PC questions were
assessed using chi-square and nonparametric methods including
the Wilcoxon 2-sample and Kruskal-Wallis tests. These methods
take into account the non-normal response distributions to the
ordinal scales used for the PC numeric questions. SAS, version
9.2, was used for all statistical analyses. If the test for overall
differences in responses across practice regions was significant
(P ≤ .05), pairwise comparisons were used to compare the
responses of each pair of regions at a more stringent level
(P ≤ .016) in order to correct for multiple testing bias.
Results
In total, 534 surveys were returned for analysis. The overall response rate was 7% (5% SNO, 6% EANO, and 15% ASNO)
(Fig. 1). Four surveys were excluded because the respondents
did not see any patients (MD, n ¼ 1; RN, n ¼ 3). The results of
nurse/nurse practitioner surveys (n ¼ 46) will be reported
separately.
Demographics
Four hundred seventy-six physician surveys were analyzed. Respondents were recategorized according to their practices into
one of 3 regions: “Asia-Oceania,” which included participants
from Asia (China, the Indian subcontinent, Japan, South Korea)
and Australia/New Zealand (n ¼ 237); “Europe” (n ¼ 75); or “United States/Canada” (n ¼ 164). Responders from North-America
(USA-C) and Europe were more likely to be female (both 29%)
than responders from Asia-Oceania (AO) (20%; P ¼ .0969)
(Table 1). Physicians from AO were more likely to be neurosurgeons and radiation oncologists, while physicians from Europe
and USA-C were more often trained in neurology (P , .001).
USA-C providers had more subspecialty training in neurooncology, but most providers received no or minimal training in
PC independent of their region. Physicians in USA-C and Europe
saw a greater number of patients with brain tumors per week
and were more likely to practice in an academic setting than
their peers from AO.
63
Walbert et al.: International patterns of palliative care in neuro-oncology
Table 1. Demographics and responses to survey
Variable
Response
Asia-Oceania
(N ¼ 237)
Europe
(N ¼ 75)
United States/
Canada
(N ¼ 164)
Sex
Male
Female
Neurology
Medical oncology
Neurosurgery
Radiation oncology
Other
No formal specialty
training
Attendance at courses,
CME lectures, and
conferences
Formal rotation during
residency, fellowship
≥6 months formal training
No formal specialty
training
Attendance at courses,
CME lectures, and
conference
Formal rotation during
residency/ fellowship
≥6 months formal training
,1
1 –5
5 –15
.15
,5 years
5 –10 years
10– 15 years
.15 years
Academic
Private/group/solo
Diagnosis
Recurrent disease
End of life
Onset of symptoms
requiring palliation
Other
0%
1%– 25%
26%–50%
51%–75%
76%–100%
0%
1%– 25%
26%–50%
51%–75%
76%–100%
188 (80%)
48 (20%)
2 (1%)
12 (5%)
86 (36%)
136 (57%)
1 (0%)
42 (18%)
53 (71%)
22 (29%)
30 (40%)
14 (19%)
16 (21%)
14 (19%)
1 (1%)
5 (7%)
117 (71%)
47 (29%)
44 (27%)
30 (18%)
48 (29%)
22 (13%)
20 (12%)
16 (10%)
97 (41%)
41 (55%)
40 (24%)
69 (29%)
11 (15%)
32 (20%)
29 (12%)
73 (31%)
18 (24%)
31 (41%)
76 (46%)
63 (38%)
107 (45%)
34 (45%)
62 (38%)
51 (22%)
4 (5%)
35 (21%)
6 (3%)
43 (18%)
120 (51%)
44 (19%)
30 (13%)
78 (33%)
50 (21%)
27 (12%)
78 (33%)
140 (59%)
97 (41%)
19 (8%)
27 (11%)
37 (16%)
138 (58%)
6 (8%)
0 (0%)
15 (20%)
36 (48%)
24 (32%)
9 (12%)
10 (13%)
22 (29%)
34 (45%)
63 (84%)
12 (16%)
7 (9%)
2 (3%)
15 (20%)
43 (57%)
4 (2%)
7 (4%)
49 (30%)
53 (32%)
55 (34%)
68 (41%)
24 (15%)
22 (13%)
50 (30%)
131 (80%)
33 (20%)
5 (3%)
16 (10%)
28 (17%)
90 (55%)
12 (5%)
8 (3%)
124 (52%)
60 (25%)
32 (14%)
10 (4%)
57 (24%)
139 (59%)
19 (8%)
12 (5%)
7 (3%)
5 (7%)
1 (1%)
22 (29%)
16 (21%)
21 (28%)
14 (19%)
6 (8%)
42 (58%)
11 (15%)
9 (13%)
4 (6%)
17 (10%)
2 (1%)
69 (42%)
35 (21%)
28 (17%)
22 (13%)
5 (3%)
31 (20%)
21 (14%)
30 (19%)
68 (44%)
Specialty
Formal training in Neuro-oncology
Formal training in palliative care
Patients with brain tumors seen per week
Practicing independently
Practice setting
I refer patients to palliative care/
symptom management at the
moment of:
What percentage of all of your patients
are referred to palliative care/
symptom management at any time
during the course of the disease?
What percentage of all of your patients
are referred to hospice for end-of-life
care?)
P valuea
.0969
Pairwise
Comparisonb
+
,.0001
*+
,.0001
X+
.1426
,.0001
*+
.0001
*X
,.0001
*+
.0802
,.0001
*+
,.0001
*X+
Continued
64
Neuro-Oncology Practice
Walbert et al.: International patterns of palliative care in neuro-oncology
Table 1. Continued
Variable
Response
Asia-Oceania
(N ¼ 237)
Europe
(N ¼ 75)
I feel comfortable dealing with endof-life issues on my own without the
need for a formal palliative care
support service?
Strongly agree
Agree
Neutral
Disagree
Strongly disagree
Strongly agree
Agree
Neutral
Disagree
Strongly disagree
Strongly agree
Agree
Neutral
Disagree
Strongly disagree
Strongly agree
Agree
Neutral
Disagree
Strongly disagree
17 (7%)
57 (24%)
53 (23%)
82 (35%)
26 (11%)
31 (13%)
116 (50%)
54 (23%)
27 (12%)
6 (3%)
17 (7%)
41 (18%)
56 (24%)
96 (41%)
24 (10%)
35 (15%)
94 (41%)
53 (23%)
39 (17%)
11 (5%)
12 (17%)
16 (22%)
11 (15%)
23 (32%)
10 (14%)
14 (19%)
32 (44%)
10 (14%)
13 (18%)
3 (4%)
7 (10%)
10 (14%)
9 (13%)
31 (43%)
15 (21%)
12 (17%)
27 (38%)
13 (18%)
16 (22%)
4 (6%)
Strongly agree
Agree
Neutral
Disagree
Strongly disagree
Strongly agree
Agree
Neutral
Disagree
Strongly disagree
Strongly agree
Agree
Neutral
Disagree
Strongly disagree
Strongly agree
Agree
Neutral
Disagree
Strongly disagree
Strongly agree
Agree
Neutral
Disagree
Strongly disagree
40 (17%)
83 (36%)
39 (17%)
57 (24%)
14 (6%)
36 (16%)
94 (41%)
39 (17%)
54 (24%)
6 (3%)
19 (8%)
70 (30%)
44 (19%)
70 (30%)
27 (12%)
8 (4%)
102 (45%)
57 (25%)
51 (22%)
10 (4%)
82 (35%)
108 (46%)
30 (13%)
10 (4%)
3 (1%)
18 (25%)
27 (38%)
13 (18%)
10 (14%)
3 (4%)
12 (17%)
31 (43%)
17 (24%)
8 (11%)
4 (6%)
11 (15%)
31 (44%)
15 (21%)
9 (13%)
5 (7%)
1 (1%)
17 (24%)
17 (24%)
30 (43%)
5 (7%)
20 (28%)
21 (30%)
20 (28%)
7 (10%)
3 (4%)
Our unit assesses symptom burden and
quality of life on a routine basis
Our unit routinely utilizes palliative
medicine professionals at the time of
first diagnosis for our high-grade
primary brain tumor patients (WHO
grades III and IV)
Our unit routinely utilizes palliative
medicine professionals when our
high-grade primary brain tumor
patients (WHO grades III and IV)
develop an increased symptom
burden
My patients have easy referral access to
inpatient palliative care services
My patients have easy referral access to
outpatient palliative care services
My patients have easy access to hospice
services
Patients’ expectations for ongoing
therapies hinder my ability to offer
palliative medicine referral
As a brain tumor specialist, I would prefer
a service called supportive care rather
than palliative care
P valuea
Pairwise
Comparisonb
30 (19%)
54 (35%)
27 (17%)
36 (23%)
9 (6%)
47 (30%)
71 (46%)
15 (10%)
17 (11%)
5 (3%)
9 (6%)
19 (12%)
25 (16%)
68 (44%)
32 (21%)
24 (15%)
68 (44%)
23 (15%)
35 (23%)
5 (3%)
,.0001
+
.0012
+
.0059
+
56 (36%)
51 (33%)
16 (10%)
22 (14%)
10 (6%)
43 (28%)
61 (39%)
24 (15%)
19 (12%)
8 (5%)
60 (39%)
59 (38%)
12 (8%)
18 (12%)
5 (3%)
6 (4%)
39 (25%)
47 (31%)
44 (29%)
17 (11%)
29 (19%)
64 (41%)
30 (19%)
28 (18%)
5 (3%)
.0003
United States/
Canada
(N ¼ 164)
.8900
+
.0215c
,.0001
*X+
,.0001
*+
,.0001
*+
a
Overall P value with significance P , .05.
Pairwise comparisons, with significance P ≤ .016.
c
Overall P value significant; however, pairwise comparisons not significant.
*Significant difference in response patterns between Asia-Oceania and Europe.
X, significant difference in response patterns between Europe and the United States/Canada.
+, significant difference in response patterns between Asia-Oceania and the United States.
b
Neuro-Oncology Practice
65
Walbert et al.: International patterns of palliative care in neuro-oncology
Figure 1. Survey results.
Response Pattern
End-of-life Care
When assessing response patterns, statistically significant differences among regions were most often seen between physicians
from AO and USA-C (14/22 questions) and AO and Europe (9/22
questions). Significant response deviations were seen less often
between European and USA-C practitioners (4/22 questions).
There were significant differences between all 3 regions regarding
hospice referral patterns (P , .0001). USA-C practitioners indicated the highest percentage of patients being referred to hospice,
while those from AO indicated the lowest percentage, with responders from Europe indicating a percentage in between. Responders from USA-C strongly agreed that they felt comfortable
dealing with end-of-life issues compared with responders from
AO. There was an overall significant difference among different
provider groups regarding this topic (P , .0001). However, when
looking at specific regions, these differences remained significant
only in USA-C practitioners. Neurosurgeons felt less comfortable
dealing with end-of-life issues compared with the neurologist
and medical oncologist groups (P , .002; Table 2).
When asked about easy access to hospice services, there were
significant differences between USA-C and Europe, USA-C and AO,
and Europe and AO: Practitioners from USA-C most often reported
that their patients had easy access to hospice services compared
with responders from Europe. Physicians from Europe mostly
agreed or felt neutral about their patients’ ease of access to hospice, while responders from AO were more likely to disagree that
their patients had easy access to hospice (P , .001).
Palliative Care
Responders from USA-C agreed more strongly that their units assess symptom burden and quality of life on a routine basis compared with responders from AO. In separate questions, physicians
were asked how their units or institutions utilize PC. Physicians
from all 3 regions agreed that their units most often utilized routinely PC when high-grade primary brain tumor patients (WHO
grade III and IV) developed increased symptom burden. However, units in USA-C were even less likely than units in AO to refer
patients to palliative medicine professionals at the time of first
diagnosis (P ¼ .0059).
Physicians practicing in the USA-C agreed more strongly that
their patients have easy referral access to inpatient PC services
compared with responders from AO, but there was no overall difference regarding access to outpatient PC in the 3 regions.
Providers from all regions agreed that they would refer patients to PC or symptom management at the onset of the observed need for palliation (55% – 58%) or in the end-of-life
setting (16% – 20%). However, responders from Europe and
USA-C indicated referring a larger overall proportion of their patients to PC when compared with AO physicians (37% and 30%,
respectively, vs 18%; P , .0001).
Practitioners in AO more often than responders from Europe
and USA-C thought that their patients’ expectations for ongoing
therapies hindered their ability to offer a referral to PC. When
asked if they would prefer a service with the name “supportive
care” rather than “palliative care,” the responders from AO significantly preferred supportive care over palliative care when compared with responders from USA-C and Europe (P , .001).
66
Discussion
Even with the limited responses from a large sample population,
this stands as the first study to assess international practice patterns of PC utilization in neuro-oncology. It represents a unique
collaboration of the 3 major professional societies caring for
brain tumor patients.
Our survey detected multiple differences in the ways PC and
hospice are perceived and utilized in the field of neuro-oncology.
The most distinct differences were found between USA-C/Europe
and the AO region. Despite these different response patterns,
physicians in all 3 regions agreed on utilizing PC at the development of increased tumor burden. In addition, our study showed
that there are significant differences in the specialties of providers
caring for brain tumor patients. It is unclear if this difference in
Neuro-Oncology Practice
Walbert et al.: International patterns of palliative care in neuro-oncology
Table 2. Feeling comfortable dealing with end-of-life issues. Mean ratings, stratified by region and medical specialty. P values based on Kruskall-Wallis
test
Medical Specialty
Region
Total Mean (SD)
Neurology & Medical Oncology,
Mean (SD)
Neurosurgery, Mean (SD)
Radiation Oncology,
Mean (SD)
P value
Asia -Oceania
Europe
North America
Total
236 3.2 (1.14)
74 3.1 (1.32)
144 2.6 (1.20)
454 3.0 (1.22)
14 2.9 (1.35)
44 3.0 (1.25)
74 2.3 (1.15)
132 2.6 (1.24)
86 3.2 (1.15)
16 3.6 (1.40)
48 3.1 (1.14)
150 3.2 (1.17)
136 3.2
14 2.7
22 2.7
172 3.1
.623
.201
.002
,.0001
demography is a reflection of how brain tumor physicians are organizing themselves in professional societies in each region or if
this variation truly reflects that brain tumor care is delivered differently in these health care systems. Other responses that underline the different ways of delivering brain tumor care are
that USA-C and European physicians see more brain tumor patients per week and more often practice in an academic setting
(both: P , .0001). The USA-C system is known for its high level
of subspecialization,16 which might explain why significantly
more USA-C physicians in our survey have 6 or more months of
formal training in neuro-oncology than in the Europe or AO. However there are no significant differences in the PC training that
might explain differences in the approach to PC in the different
regions. Between 31% and 41% of all participants have received
no formal training in PC, and most physicians (38%– 45%) have
attended only courses, CME lectures, or conferences rather than
having PC training as an integral part of their specialty training.
Most of the differences in practice patterns were observed between USA-C and AO or Europe and AO. The only statistically significant difference between Europe and USA-C, other than some
demographic statistics, occurred regarding hospice care. USA-C
physicians responded that they referred patients more frequently
to hospice for end-of-life care, and USA-C providers think that
they have easier access to hospice services than their European
counterparts (both: P , .0001). On the other hand, European physicians mostly agreed or felt neutral about their patients’ ease of
access to hospice, while responders from Asia were more likely to
disagree that their patients had easy access to hospice (P , .001).
While it is generally known that access to PC and hospice is more
limited in the AO region (with the exception of Australia and New
Zealand, where the approach to PC is more similar to Europe and
USA-C),17 – 19 we found it surprising that there was a perceived difference in access to hospice care in European countries when
compared with USA-C. While the European and the North American countries are thought to have high-level access to symptom
management and end-of-life care,19 it must be noted that there
are significant differences in how PC and end-of-life care for brain
tumor patients are delivered in different European countries
based on their health care systems.20,21 A comparison of
end-of-life care for brain tumor patients between 3 European
countries showed that more than twice as many patients were
enrolled in hospice when dying in the UK (42%) than in Austria
(16%) or the Netherlands (15%).21
USA-C neurosurgeons felt significantly more uncomfortable
dealing with end-of-life issues than their counterparts in other
Neuro-Oncology Practice
(1.12)
(1.44)
(1.16)
(1.16)
regions. We speculate that this notion might be caused by the
specialization process in USA-C, which favors reliance on neurooncologists for deliverance of longitudinal care after the original
resection (Table 2). However, a historic survey of US neurologists
revealed that neuro-oncologists might not be very well prepared
to facilitate end-of-life decision-making.22
It is important to point out that there was general agreement
by individual providers, across continents and specialties, to refer
patients when they started to develop increased symptom burden. This response was validated by a similar response in a separate question in our survey asking about the referral patterns of
institutions as well as individual physicians. More than half of all
respondents thought that their unit would involve PC on a routine
basis at the moment symptoms required palliation. Consistent
with this referral pattern, there was general agreement of practitioners not to refer patients to PC at the time of first diagnosis of a
high-grade brain tumor.
When differentiating the referral patterns of individual providers and institutions as a whole, the individuals showed a much
stronger preference for later referral. While only 3%–9% of individuals endorsed referring patients to PC at the time of diagnosis,
up to 18% – 25% of respondents agreed that their institutional
approach would be to refer patients to PC at initial diagnosis.
This finding is crucial because there have been increasing efforts
to provide PC earlier in the disease trajectory and not to wait until
the end of life to involve hospice.23 In a landmark randomized
study, Temel et al showed that patients with metastatic lung
cancer had meaningful improvements in quality of life, symptom
burden, mood, and even prolonged survival when they received
early PC.7 While there is no official position from one of the European or Asian cancer societies, this approach has been endorsed
by the American Society of Clinical Oncology.9 However, it is unclear if brain tumor patients would benefit in similar ways since
they suffer from different symptoms than patients with metastatic lung cancer.12 The majority of brain tumor patients show
signs of drowsiness (85% – 90%), poor communication (64% –
90%), focal neurological deficits (51% – 62%), and seizures
(30%– 56%) in the end-of-life phase,12 while systemic cancer patients are mainly affected by fatigue, weight loss, appetite loss,
weakness, and pain.24 In one study, 52% of brain tumor patients
were not thought to be competent by their treating physicians
in the weeks prior to death. This number increased to 85% in
the final week of life.25 Based on these symptoms, brain tumor
patients might benefit from early involvement of PC to facilitate end-of-life planning and to pursue proactive symptom
67
Walbert et al.: International patterns of palliative care in neuro-oncology
management. However, our survey implies that the early involvement of PC teams does not play a major role in neuro-oncology at
this time.
We found significant differences in referral patterns to hospice
between the 3 regions. While the majority of patients in USA-C are
referred to hospice, fewer than 25% of patients in AO and Europe
are referred to hospice. One of the reasons might be the limited
access to hospice in some of these regions. While more than
three-quarters of USA-C physicians reported easy access to hospice, fewer providers agreed with this statement in Europe (59%)
and AO (38%). This limitation in access is especially noteworthy,
given that almost half of all physicians in the AO and European
regions did not feel comfortable dealing with end-of-life issues
on their own. In addition to limitations in training and access, cultural differences might influence the involvement of PC and hospice care. Almost half of respondents from the ASNO region (49%)
thought that patient expectations for ongoing therapies might
hinder their ability to offer a referral to PC. This notion is quite different in Europe (50%) and USA-C (40%), where physicians did not
think that patient expectations would impair their ability to refer
to PC. Cultural differences, fear of abandonment, and limited
knowledge about PC are known barriers in some of the AO regions.17,18,26 This barrier to patient referral to PC might be lowered
by a name change from palliative care to supportive care since a
strong majority of respondents agreed with such a name change
(58% – 80%). This notion has been shared in at least one other
survey. Oncology providers in one major cancer center perceived
the name palliative care to be more distressing and thought that
it would reduce hope for patients and families.15 A later name
change from palliative care to supportive care was associated
with increased referrals and earlier access to PC.14 Given the
limited survival of brain tumor patients and their reluctance to
embrace PC services, increasing formal PC training for neurooncology providers, or at least increasing access to PC and hospice, appears to be an important step towards improving the
quality of life for brain tumor patients.
Our survey has several limitations that should be acknowledged. First, a minority of SNO, ASNO, and EANO members responded to this survey. It is generally known that the response
rate to electronic surveys can be increased by repeated e-mail invitations and providing incentives.27 Based on the setup of the
SNO database and society policies, we were unable to send repeat invitations or track specific participants to provide incentives.
Given that the survey was sent not only to clinicians but also to all
participants of the annual SNO meeting, it included basic researchers as well as translational scientists and mid-level providers. The results were limited to physicians only to minimize this
bias, which further decreased the response rate. The EANO survey
did not utilize an electronic online survey tool, which might have
decreased the response rate since participants needed to return
results by e-mail or fax, which required additional steps of work.
These additional challenges might have caused overrepresentation of physicians with interest and experience in PC in our
study. Given these limitations, the response rate is similar to another survey in the field of neuro-oncology that investigated practice patterns of treatment and diagnosis of intracranial radiation
necrosis. That survey had a response rate of 9%, but the organizers were able to send follow-up emails to nonresponders.28 Another earlier SNO survey of their members, which investigated
treatment approaches to anaplastic oligodendroglioma, reached
68
a 20% response rate, but again it was targeted more to members
and clinicians than our survey.29 Given that only a minority responded to the surveys, actual clinical practice might not be
completely reflected by these results, and physicians with special
interest in and experience in PC might be overrepresented in our
study. Anticipating this bias, we asked not only about the individual physician’s practice pattern but also asked for details regarding the institution’s approach.
Beyond these limitations, our survey gives important insight
into how neuro-oncological care is delivered globally and how
practitioners utilize PC and hospice services. Further research
evaluating access to care on a national and international level,
which would correlate the quality of care as well as patients’ quality of life and satisfaction with different patterns of care delivery,
will be of tremendous importance for the future.
Funding
Department of Neurosurgery and the Hermelin Brain Tumor Center, Henry
Ford Health System (T.W., A.R.T.), Vattikuti Foundation (T.W.), and NCI
K24CA160777 (V.K.P.).
Acknowledgments
The authors wish to thank Dr. Michael Glantz and Dr. Eduardo Bruera for
their assistance in creating the study questionnaire. We would also like to
thank Charles Haynes and Megan Bell of the Society for Neuro-Oncology
and the Brain Tumour Foundation of India for their help facilitating this
survey and Susan MacPhee for her editorial assistance. And finally, we
thank the survey participants for taking the time to share their experience.
Conflict of interest statement. None declared.
References
1.
Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus
concomitant and adjuvant temozolomide for glioblastoma. N Engl
J Med. 2005;352(10):987–996.
2.
Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med. 2008;
359(5):492 –507.
3.
Prados MD, Seiferheld W, Sandler HM, et al. Phase III randomized
study of radiotherapy plus procarbazine, lomustine, and vincristine
with or without BUdR for treatment of anaplastic astrocytoma:
final report of RTOG 9404. Int J Radiat Oncol Biol Phys. 2004;58(4):
1147 –1152.
4.
van den Bent MJ, Carpentier AF, Brandes AA, et al. Adjuvant
procarbazine, lomustine, and vincristine improves progression-free
survival but not overall survival in newly diagnosed anaplastic
oligodendrogliomas and oligoastrocytomas: a randomized European
Organisation for Research and Treatment of Cancer phase III trial.
J Clin Oncol. 2006;24(18):2715–2722.
5.
World Health Organization. WHO definition of palliative care.
Available at http://www.who.int/cancer/palliative/definition/en/.
Accessed August 8, 2014.
6.
Meier DE, Brawley OW. Palliative care and the quality of life. J Clin
Oncol. 2011;29(20):2750– 2752.
7.
Temel JS, Greer JA, Muzikansky A, et al. Early palliative care for
patients with metastatic non– small-cell lung cancer. N Engl J Med.
2010;363(8):733–742.
Neuro-Oncology Practice
Walbert et al.: International patterns of palliative care in neuro-oncology
8.
MedlinePlus. Definition of hospice. Available at www.nlm.nih.gov/
medlineplus/hospicecare.html. Accessed August 8, 2014.
9.
Smith TJ, Temin S, Alesi ER, et al. American Society of Clinical
Oncology provisional clinical opinion: the integration of palliative
care into standard oncology care. J Clin Oncol. 2012;30(8):880– 887.
10.
Gaertner J, Wolf J, Hallek M, Glossmann JP, Voltz R. Standardizing
integration of palliative care into comprehensive cancer therapy--a
disease specific approach. Support Care Cancer. 2011;19(7):
1037 –1043.
19.
Lynch T, Connor S, Clark D. Mapping levels of palliative care
development: a global update. J Pain Symptom Manage. 2013;
45(6):1094 –1106.
20. Centeno C, Clark D, Lynch T, et al. Facts and indicators on palliative
care development in 52 countries of the WHO European region:
results of an EAPC Task Force. Palliat Med. 2007;21(6):463 –471.
21.
Koekkoek JA, Dirven L, Reijneveld JC, et al. End of life care in
high-grade glioma patients in three European countries: a
comparative study. J Neurooncol. 2014;120(2):303– 310.
Sizoo EM, Pasman HR, Dirven L, et al. The end-of-life phase of
high-grade glioma patients: a systematic review. Support Care
Cancer. 2014;22(3):847– 857.
22.
Carver AC, Vickrey BG, Bernat JL, Keran C, Ringel SP, Foley KM.
End-of-life care: a survey of US neurologists’ attitudes, behavior,
and knowledge. Neurology. 1999;53(2):284–293.
12. Walbert T, Khan M. End-of-life symptoms and care in patients with
primary malignant brain tumors: a systematic literature review.
J Neurooncol. 2014;117(2):217 –224.
23.
Greer JA, Jackson VA, Meier DE, Temel JS. Early integration
of palliative care services with standard oncology care for
patients with advanced cancer. CA Cancer J Clin. 2013;63(5):
349–363.
24.
Teunissen SC, Wesker W, Kruitwagen C, de Haes HC, Voest EE,
de Graeff A. Symptom prevalence in patients with incurable
cancer: a systematic review. J Pain Symptom Manage. 2007;34(1):
94– 104.
25.
Sizoo EM, Pasman HRW, Buttolo J, et al. Decision-making in the
end-of-life phase of high-grade glioma patients. Eur J Cancer.
2012;48(2):226 –232.
11.
13.
14.
Ford E, Catt S, Chalmers A, Fallowfield L. Systematic review of
supportive care needs in patients with primary malignant brain
tumors. Neuro Oncol. 2012;14(4):392– 404.
Dalal S, Palla S, Hui D, et al. Association between a name change
from palliative to supportive care and the timing of patient
referrals at a comprehensive cancer center. Oncologist. 2011;16(1):
105– 111.
15. Fadul N, Elsayem A, Palmer JL, et al. Supportive versus palliative care:
what’s in a name?: a survey of medical oncologists and midlevel
providers at a comprehensive cancer center. Cancer. 2009;115(9):
2013 –2021.
16. Vaillant B, Kuo SH, de Groot J. Emerging subspecialties in neurology:
neuro-oncology: a developing subspecialty with many opportunities.
Neurology. 2009;72(11):e51– e53.
17.
Khosla D, Patel FD, Sharma SC. Palliative care in India: current
progress and future needs. Indian J Palliat Care. 2012;18(3):
149–154.
18.
Li J, Davis MP, Gamier P. Palliative medicine: barriers and
developments in mainland China. Curr Oncol Rep. 2011;13(4):
290 – 294.
Neuro-Oncology Practice
26. Li X, Xing YF, Chen ZH, Dong M, Wu XY. Palliative care in urban areas of
China. Lancet Oncol. 2013;14(9):e339.
27.
Klabunde CN, Willis GB, McLeod CC, et al. Improving the quality of
surveys of physicians and medical groups: a research agenda. Eval
Health Prof. 2012;35(4):477– 506.
28. Stockham AL, Ahluwalia M, Reddy CA, et al. Results of a questionnaire
regarding practice patterns for the diagnosis and treatment of
intracranial radiation necrosis after SRS. J Neurooncol. 2013;115(3):
469–475.
29.
Abrey LE, Louis DN, Paleologos N, et al. Survey of treatment
recommendations for anaplastic oligodendroglioma. Neuro Oncol.
2007;9(3):314– 318.
69