Documente Academic
Documente Profesional
Documente Cultură
Correspondence: Dr. Mohamad Abdurrahman Tayeb · Hematology & Oncology Center, North West Armed Forces Hospitals, PO Box 100,
Tabuk, Saudi Arabia · drtayebweb@hotmail.com · Submitted: December 2009 Accepted: March 2010
BACKGROUND AND OBJECTIVES: Twelve “good death” principles have been identified that apply to
Westerners. This study aimed to review the TFHCOP good death perception to determine its validity for Muslim
patients and health care providers, and to identify and describe other components of the Muslim good death
perspective.
SUBJECTS AND METHODS: Participants included 284 Muslims of both genders with different nationalities and
careers. We used a 12-question questionnaire based on the 12 principles of the TFHCOP good death definition,
followed by face-to-face interviews. We used descriptive statistics to analyze questionnaire responses. However,
for new themes, we used a grounded theory approach with a “constant comparisons” method.
RESULT: On average, each participant agreed on eight principles of the questionnaire. Dignity, privacy, spiri-
tual and emotional support, access to hospice care, ability to issue advance directives, and to have time to say
goodbye were the top priorities. Participants identified three main domains. The first domain was related to faith
and belief. The second domain included some principles related to self-esteem and person>s image to friends
and family. The third domain was related to satisfaction about family security after the death of the patient.
Professional role distinctions were more pronounced than were gender or nationality differences.
CONCLUSION: Several aspects of «good death,» as perceived by Western communities, are not recognized as
being important by many Muslim patients and health care providers. Furthermore, our study introduced three
novel components of good death in Muslim society.
T
he basic duty of health care providers is to Kubler-Ross and Raymond Moody: “Looking deeply
preserve human health and life, but we should into the way that we care for the dying person, they have
realize that death is the inevitable destiny of shown that with unconditional love, and a more enlight-
mankind predetermined by Allah (the creator of the ened attitude, death can be a peaceful, even transforma-
universe). In cases in which recovery is hopeless, the role tive experience.”3 However, dealing with a patient at the
of health care providers does not end but rather is modi- end of life, aiming to improve quality of life, and plan-
fied.1 Health care providers need to help patients and ning for end-of-life care requires a good understanding
families minimize suffering and maximize comfort by of that patient’s state from a medical, social, spiritual,
offering appropriate medical care that is neither exces- and psychological point of view. To date, this important
sive nor negligent. This principle cannot be applied in topic is understudied in schools of medicine, and the ex-
10% to 20% of cases in which death happens suddenly tensive literature on medical errors shows that medical
(myocardial infarction, arrhythmia, intracranial bleed- experts are rarely blamed for “bad” deaths.4 The authors
ing, aortic dissection, accident), but in 80% to 90% of of the final report on The Future of Health and Care of
cases, in which death is predicted,2 both the patient and Older People (TFHCOP) have identified 12 principles
the medical team are aware of its imminence. This is of a good death (Table 1).5,6
known as anticipated death, which must be planned if Most of the conducted studies examined the concept
all goes well. of good death in elderly whites, but no comparable qual-
The whole subject of death and dying has been ad- itative data exist regarding other races.7 No qualitative
dressed in the West by pioneers such as Elisabeth study has been conducted in a Muslim society, and pub-
Table 1. Principles of a end-of-life care according to the report, Hematology and Oncology Center, especially those with
The Future of Health and Care of Older People.
advanced malignancy or those who were under palliative
1. To know when death is coming, and to understand what care. Death is a multi-dimensional process that involves
can be expected.
physical symptom management as well as certain reli-
2. To be able to retain control of what happens. gious, social, and psychological needs of the dying and
3. To be afforded dignity and privacy. their loved ones.14 Non-physical issues may differ widely,
which can be attributed mainly to religious and cultural
4. To have control over pain relief and other symptom control.
differences. Therefore, we expected that Muslim partici-
5. To have choice and control over where death occurs (at pants may perceive these issues in a completely different
home or elsewhere).
manner. Approval of the study was obtained from the
6. To have access to information and expertise of whatever local research ethics committee.
kind is necessary.
Each participant was interviewed as well as adminis-
7. To have access to any spiritual or emotional support tered a questionnaire. Before they were administered the
required.
questionnaire, they were made privy to the nature of the
8. To have access to hospice care in any location, not only in research and its purpose by asking the following ques-
hospital.
tions: 1) What constitutes a good death and a bad one?
9. To have control over who is present at the time when the 2) Can we develop our own definitions in keeping with
end comes.
our religious principles and cultural values? 3) Is this 12-
10. To be able to issue advance directives, which ensure principle definition valid as a definition of a good death in
wishes are respected.
Islamic culture? 4) Please express your opinions freely. Do
11. To have time to say goodbye, and control over other not be influenced by others’ opinions. 5) Share your own
aspects of timing.
experiences and feelings, and not what you have heard
12. To be able to leave when it is time to go, and not to have from others. 6) Express your opinions. There is no wrong
life prolonged pointlessly.
or right answer. 7) We would like to know your opinions.
We developed a questionnaire on the basis of the
TFHCOP’s “12 principles of a good death.” The ques-
lished papers on this important topic have focused main- tionnaire comprised 12 closed-ended questions to which
ly on reviewing Islamic teachings and the literature.8 the participants had to answer in “Yes” or “No.” The ques-
The purpose of this study was to review the tionnaires were provided in Arabic or English, depend-
TFHCOP perception of good death to determine its va- ing on the participants’ preferences (Appendices 1, 2). To
lidity for Muslim patients and health care providers and ensure the validity of the questionnaire, before conduct-
to identify and describe other elements for a good death. ing the main interviews, we analyzed the questionnaire
We tried to elaborate on the concept of good death in in both languages with 10 participants of different sub-
our society. The Western definition of “good death” was groups. We ensured that the questions were simple and
chosen rather than the Ghanaian or Tibetan one since easy to understand, so that the respondents did not have
our medical practice depends mainly on Western refer- any difficulty in interpreting and answering the questions.
ences; however, there should be some degree of flexibility Some participants, however, had difficulty in choosing a
in applying the Western perspective since death beliefs reply to a few questions. In such cases, we clarified the
have religious and cultural backgrounds. questions and explained each option by giving examples.
We then let them determine how essential they found the
SUBJECTS AND METHODS point and to choose their answer accordingly.
Participants were recruited by a random sampling tech- We used a qualitative approach to draw out previ-
nique per category from King Abdul-Aziz Military ously unexplored aspects and components of the Muslim
Hospital and from a rehabilitation center and long-stay perspective. We conducted in-depth, open-ended, and
nursing unit in King Khalid Military Hospital in Tabuk. face-to-face interviews and content analysis. We did not
Since most people die surrounded by medical profes- impose any theoretical assumptions a priori and instead
sionals, even when dying occurs at home, a full spectrum let the participants suggest any principles that they con-
of persons involved with end-of-life care-physicians, sidered to be essential.
nurses, social workers, religious officers, patients with After completing the questionnaire, the participants
life-limiting diseases, and their home caregivers (fam- were asked to express and write their opinions on the
ily members) were included in the survey.12,13 Patients principles (not included in the previous 12 points) that
and family members were recruited mainly from the constitute a good death. We convened focus groups, each
Career
Sex Nationality
Total Health care Health care Patients
providers providers
Males Females Saudi Non-Saudi Group 1 Group 2
Principle 1: Timing of death 80 (28%) 48 (29%) 32 (27%) 41 (28%) 39 (28%) 50 (28%) 24 (31%) 26 (23%)
Principle 2: Control of what
177 (62%) 99 (60%) 78 (65%) 90 (61%) 87(64%) 115(64%) 47(61%) 16 (62%)
happens
Principle 3: Dignity and privacy 271 (95%) 156 (95%) 115 (96%) 144 (98%) 127 (93%) 176 (97%) 71 (92%) 24 (92%)
Principle 4: Pain and other
246 (87%) 141 (86%) 105 (88%) 132 (90%) 114 (83%) 163 (90%) 60 (78%) 23 (88%)
symptom relief
Principle 5: Where death
127 (45%) 70 (43%) 57 (48%) 70 (47%) 57 (41%) 86 (48%) 30 (39%) 11 (42%)
occurs
Principle 6: Access to
116 (41%) 50 (30%)* 66 (55%)* 63 (43%) 53 (39%) 82 (45%)* 21 (27%)* 13 (50%)*
necessary information
Principle 7: Spiritual or
255 (90%) 146 (89%) 109 (91%) 135 (92%) 120 (88%) 166 (92%) 66 (86%) 23 (88%)
emotional support
Principle 8: Access to hospice
255 (90%) 144 (88%) 111 (93%) 135 (92%) 120 (88%) 165 (91%) 66 (86%) 24 (92%)
care
Principle 9: Control over who is
108 (38%) 64 (39%) 44 (37%) 59 (40%) 49 (36%) 71 (39%) 30 (39%) 7 (27%)
present
Principle 10: To issue advance
240 (85%) 139 (85%) 101 (84%) 126 (40%) 114 (83%) 155 (86%) 63 (82%) 22 (85%)
directives
Principle 11: To say goodbye 209 (74%) 119 (73%) 90 (75%) 108 (73%) 99 (72%) 133 (73%) 57 (74%) 19 (73%)
Principle 12: To leave when it is
207 (73%) 110 (75%) 97 (71%) 109 (74%) 98 (72%) 137 (76%) 50 (65%) 20 (77%)
time to go
comprising two to seven participants, over a 2-month pe- 37 years). The study sample consisted of 164 males (58%)
riod. The interviews usually lasted for around 30 minutes and 120 females (42%). The study included participants
per group. of several different nationalities: 147 Saudi (52%), 42
Univariate descriptive statistics (frequencies, percent- Egyptian (15%), 23 Syrian (8%), 17 Pakistani (6%), 12
ages) were used to analyze responses to each point of the Sudanese (4%), 11 Filipino (4%), 11 Jordanian (4%), 10
questionnaire. Percentages are reported as whole num- Malaysian (4%), 7 Indian (3%), 2 South African (1%),
bers. For bivariate analysis, differences in participant char- 1 Moroccan (<1%), and 1 Nigerian (<1%). The most
acteristics among different questions were determined by common groups among the participants were 93 nurses
using the chi-square test. P values of <.05 were consid- (33%), 88 physicians (31%), 43 patients’ relatives (15%),
ered statistically significant. For new themes we followed 26 patients (9%), 16 social workers (6%), 14 clinical
a grounded theory approach with a “constant compari- pharmacists (5%), and 4 hospital religious officers (1%).
sons” method and its related open and axial coding tech- Some focus group members were concerned about our
niques.9,10 Trustworthiness was noted when participants society’s tendency to consider death as taboo, something
respond affirmatively to researchers’ interpretations.11 that human beings cannot interfere with. Participants in-
formed us of cases in which health care providers avoided
RESULTS end-of-life discussions because they believed that it is be-
Researchers interviewed 284 participants. Focus group yond our control as humans.
participants ranged in age from 18 to 71 years (mean age, On average, each participant agreed with the eight
Principles
Self-esteem and body image
The second domain includes some principles related to
Figure 1. Percentage of responses to each principle by group.
the patient’s self-esteem and image in his friends’ and
relatives’ eyes, by avoiding post-mortem distortions,
deformities, septic wounds, or bad odors by maintain-
Table 3. Principles of a good death from the Muslim perspective. ing continence and keeping the body and clothes free of
· Aspects related to faith and relationship with Allah urine, stool, and vomit, and making sure the body has a
normal appearance after death.
· Aspects related to self-esteem and person’s image in the eyes of relatives
· Aspects related to concerns about family security Concerns about family security
· To be afforded dignity and privacy The third domain is related to the patient’s satisfaction
about his relatives. In other words, he needs to feel that
· To have access to any spiritual or emotional support required
his family will be secure and have no trouble after his
· To have access to hospice care in any location, not only in hospital death, so he will not be worried about them. This relates
· To be able to have control over pain relief and other symptom control primarily to economic and social concerns.
It is worth mentioning that data obtained from a
· To be able to issue advance directives, which ensure wishes are respected
sub-group of Saudis reflected the same eight principles
· To have time to say goodbye and control over other aspects of timing selected by major subgroups including females, health
· To be able to leave when it is time to go, and not to have life prolonged pointlessly care professionals (Group 1), non-medical health care
providers (Group 2), patients’ home caregivers, and pa-
· To be able to retain control of what happens
tients themselves (Figure 1). However, the order of se-
quence of these selected eight points was slightly differ-
ent. The resultant responses were almost identical to all
principles of the questionnaire, so we selected the top questions with minimal differences among groups. On
eight as the important principles for our society. Table 2 the other hand, the three new themes reflect the com-
shows the frequencies and percentage of “yes” answers for mon ground shared by participants. However, we found
each principle according to nationality, gender, and career. remarkable differences among groups. In fact, profes-
Health care providers were categorized into two groups: sional role distinctions were more pronounced than
Group 1 included health care providers who are involved were gender or nationality differences. For example,
mainly in medical issues, i.e. physicians and nurses; most physicians and nurses were highly attuned to the
Group 2 included the other members of the multi-dis- needs of good hygiene and preservation of a patient up
ciplinary care team who are involved mainly in other as- until his last breath. Religious officers discussed faith
pects of care, i.e. patients’ relatives, social workers, clinical and spiritual support and were the only group to dis-
pharmacists, and hospital religious officers. cuss postmortem preservation of configuration. Social
Participants identified certain aspects of quality of workers’ discussions were more psychosocial in nature
death that are not mentioned in the Western literature and focused on being reassured about the family’s future
study design. A “Yes/No” question format may not be the whenever possible. They should be ready to help the pa-
best way to measure participants’ preferences in this type tient to take a bath more frequently as well. To reduce
of research. A five-point Likert scale would have been a postmortem disfigurement, jaw fixation and eye closing
better assessment tool because it would allow the partici- must be done immediately at the time of death. All pa-
pants to choose from a range of options that reflect the tients should be reassured that this is the practice with all
degree to which they agree or disagree with a statement deceased Muslims in the hospital. The rites of washing,
and also to abstain from committing themselves to one shrouding, funeral prayers, and burial should follow as
response or the other if they were not sure. Although the soon as possible. In addition to expressing empathy, the
fact that we obtained similar responses from all subgroups major role of the health care team at this stage is timely
may support test reliability, further studies are required to documentation to prevent any unnecessary delay in pro-
assess the validity of using a questionnaire for this kind of ceeding with funeral rites. Physicians should be reminded
topic. The questionnaire was provided in one of two lan- that they are not alone when caring for dying patients;
guages, which may bear the potential for inter-rater vari- many other health care providers (nurses, social workers,
ability and language translation inaccuracy. Researchers and religious officers) are available to provide comprehen-
conducted a pilot study with 10 participants who received sive care. Physicians may ask a screening question regard-
the questionnaire in one language and then in the other ing any faith-related concerns and then ask whether the
language. Proper modifications were made to ensure re- patient or relatives would like to speak in greater depth
ceipt of the same response. There was a preliminary as- with a religious officer (a Sheikh or Imam). In addition,
sumption that principles of good death among whites, the physician should ask the patient a screening ques-
as reported by a TFHCOP, are applicable to a group of tion to figure out any concerns related to his relatives
Muslim participants. This was obvious by adopting these and make sure that he has no other worries. The physi-
principles as leading questions addressed to Muslim par- cian can then consult the social worker to help him in this
ticipants. The authors suggest that similar studies can be respect. However, the palliative care team may need to
repeated using modified principles that are in better con- identify families with suboptimal resources, provide the
cordance with Islamic culture. Although our participants necessary support during bereavement, and reassure the
represented a broad range of ages, nationalities, careers, patient that his family will receive economic support after
and educational levels, all were recruited from Northwest his death. This is not the physician’s primary duty, yet he
Armed Forces Hospitals; therefore, our findings may not should explore this point and ask for proper consultation,
reflect the perceptions in other areas. A large study on a if necessary.
national or international basis may be of importance to It is important that the medical curriculum covers this
address this issue. issue in detail. The Islamic perspective of “good death” must
Our study has implications for both education and be included in health care services, professional codes, and
practice. Health care providers must understand their care plans or missions for end-of-life care organizations
patients’ preferences and respect their needs regardless and institutions in Islamic countries. This is more compli-
of what the health care provider believes. Physicians and cated than simply translating Western literature and try-
nurses should do their best to care for each patient’s ap- ing to apply it to our practice that exists in a society with
pearance and hygiene, as this is of great importance to different cultural and religious backgrounds; care must be
Muslims. This can be achieved by keeping the clothes and taken to develop such information in a Muslim-centered
body of the patient free from urine, stool, vomit, or blood manner.
Appendix 1. Questionnaire in Arabic. Appendix 2. Questionnaire in English: What do you think about
these principles? Do you think they are well-matched to your
conception of a “good death?”
OBSERVATIONAL STUDY
Abstract: The primary aim of this study was to explore common expected to care for the patient at home. At the time of death, while
beliefs and practices when death is approaching in East-Asian countries. no Japanese physicians stated that they often experienced patients
A cross-sectional survey was performed involving palliative care wanted a religious person to visit, the corresponding figure in Korean
physicians in Japan, Korea, and Taiwan. Measurement outcomes were and Taiwan was about 40%. Uncovered expression of emotion was
physician-perceived frequencies of the following when patient death significantly frequently observed in Korean and Taiwan, and 42% of the
was approaching: (1) reluctance to take part in end-of-life discussions, Japanese physicians reported family members cleaned the dead body of
(2) role of family members, (3) home death, and (4) circumstances the patient themselves.
surrounding death. There seem to be significant intercountry differences in beliefs and
A total of 505, 211, and 207 responses were obtained from Japanese, practices when death is approaching in East Asian countries. Future
Korea, and Taiwan physicians, respectively. While 50% of the Japanese studies on direct observations of patients and families are needed.
physicians reported that they often or very often experienced families as (Medicine 94(39):e1573)
being reluctant to discuss end-of-life issues, the corresponding figures
were 59% in Korea and 70% in Taiwan. Two specific reasons to avoid Abbreviation: ANOVA = analysis of variance.
end-of-life discussion, ‘‘bad things happen after you say them out loud’’
and ‘‘a bad life is better than a good death’’ were significantly more
frequently observed in Taiwan. Prioritizing the oldest of the family in INTRODUCTION
breaking bad news and having all family members present at the time of
death were significantly more frequently observed in Korea and Taiwan.
Half of Taiwanese physicians reported they often or very often experi-
A n understanding of cultural differences is very important for
providing patient- and family-centered end-of-life care.
What patients and families believe is usual or appropriate when
enced the patients/family wanted to go back home to die because the death is approaching is heavily influenced by culture, and to
soul would not be able to return from the hospital. In all countries, more provide appropriate care for imminently dying patients, an under-
than 70% of the physicians reported certain family members were standing of the culture of the patients and family members is
essential.1–4 Nonetheless, to the best of our knowledge, there
Editor: Wen-Hung Wang. have been no large-scale studies regarding what is usual when
Received: June 25, 2015; revised: July 30, 2015; accepted: August 19, death is approaching, except for review articles based on the
2015. experience of clinicians. Existing cross-cultural studies have been
From the Department of Family Medicine, College of Medicine and focused on patient autonomy, information disclosure, communi-
Hospital, National Taiwan University, Taipei, Taiwan (SYC), Department
of Family Medicine, Dongguk University Ilsan Hospital, Dongguk cation, decision-making, hydration, pain management, and with-
University School of Medicine, Seoul, South Korea (S-YS), Department drawal/withholding of life sustaining treatments.5–12
of Palliative and Supportive Care, Palliative Care Team, and Seirei East Asia is traditionally regarded as a typical family-
Hospice, Seirei Mikatahara General Hospital, Japan (TM), Division of centered region that is based on Confucian culture.4 Japan,
Clinical Psychology, Kyoto University, Kyoto, Japan (YO), Department of
Family Medicine, College of Medicine and Hospital, National Taiwan Korea, and Taiwan, however, have considerable differences in
University, Taipei, Taiwan (T-YC), Department of Hematology and cultural traditions, and each country could have unique
Oncology, Ulsan University Hospital, University of Ulsan College of traditions about death and dying. For example, several studies
Medicine, Ulsan, South Korea (SJK), Department of Social Welfare, Korea indicated that, in Taiwan, families believe that the soul will not
National University of Transportation, Chungju City, South Korea (HSK),
Department of Family Medicine, Taipei Veterans General Hospital and be able to return from the hospital if patients die in hospitals;
National Yang Ming University, School of Medicine, Taipei, Taiwan (S- this could have a great deal of influence on the patient-pre-
JH), Graduate School of Education, Kyoto University, Kyoto, Japan (TY), ferred place of death, that is, many Taiwanese want to go back
Department of Multidisciplinary Cancer Treatment, Graduate School of home to die even if they are unconscious.4,13 – 15 In Korea, it is
Medicine, Kyoto University, Kyoto, Japan (ST).
Correspondence: Shao-Yi Cheng, Department of Family Medicine, College suggested that the concept of filial piety (devotion to and
of Medicine and Hospital, National Taiwan University, 7, Chung Shan respect for parents) and strong ties among family members
S. Rd, Taipei, Taiwan (e-mail: scheng2140@gmail.com). heavily influence end-of-life decisions.4,16 – 18 In Japan, many
The authors report no conflicts of interest to disclose. identify themselves as both Buddhist and Shinto; they do not
Copyright # 2015 Wolters Kluwer Health, Inc. All rights reserved.
This is an open access article distributed under the Creative Commons attend worship services or participate in seasonal rituals for
Attribution-NonCommercial-NoDerivatives License 4.0, where it is several occasions without religious aims.4,19 – 22 In these 3
permissible to download, share and reproduce the work in any medium, countries, the situation is rapidly changing, and clarification
provided it is properly cited. The work cannot be changed in any way or of the common beliefs and practices in East Asian countries
used commercially.
ISSN: 0025-7974 when death is approaching is valuable for the provision of
DOI: 10.1097/MD.0000000000001573 culturally suitable end-of-life care.
The primary aim of this study was to explore the potential interviews. Face validity was confirmed by a pilot testing on 10
differences in common beliefs and practices when death is palliative care clinicians using qualitative format, and after
approaching, based on physician reports from these East several revisions all finally agreed questionnaires were under-
Asian countries. standable and appropriate in each country. The questionnaire
was simultaneously developed in Japanese, Korean, Taiwa-
nese, and English. For all questions, the physicians were asked
METHODS to rate the frequencies they experienced them on a Likert scale
This was a cross-sectional survey of palliative care special- of 1 (not at all), 1 (rarely), 2 (sometimes), 3 (often), to 4 (very
ists in Japan, Korea, and Taiwan. Measurement outcomes were often).
physician-perceived frequencies when patients were dying. Reluctance to take part in end-of-life discussions was
There was also an assumption that rough estimates of the investigated using 3 items: (1) family members are reluctant
frequencies were not seriously different from direct observation to discuss end-of-life issues until the patient is at the terminal
of patients. stage; (2) because ‘‘bad things happen after you say them out
loud,’’ the patient and family are reluctant to talk about a future
Subjects and Procedures worsening in the patient’s condition; and (3) because ‘‘a bad life
We distributed a questionnaire to palliative care phys- is better than a good death,’’ the patient and family are reluctant
icians. Rationale for selecting palliative care physicians for to talk about a future worsening in the patient’s condition.
this study is that physicians are reasonably reliable source of The role of family members was investigated using 3
information without burden on patients and families. Further- items: (1) when the physicians report ‘‘bad news,’’ they speak
more, palliative care physicians as data sources was highly to the oldest or head of the family first; (2) families recognize as
feasible, as they experienced many patient deaths and this proxy important that all family members are present at the last
method is reliable and common in palliative care research.23,24 moment; and (3) children want to do everything to fulfill ‘‘filial
Due to differences in specialist registry and survey feasibility piety.’’ These involve the core concepts of Confucianism, that is,
among the countries, we decided to adopt the most feasible respect for older persons and the family bond.
methods based on the actual situation in each country. All the Home death was investigated using 5 items: (1) because it
palliative care physicians in the three countries work in is believed that ‘‘the soul will not be able to return from the
the hospitals. hospital,’’ patients and their families want death to occur at
In Japan, all 605 palliative care physicians certified by the home; (2) because ‘‘death at home brings bad luck,’’ patients
Japanese Society of Palliative Medicine before June 2012 were and their families do not want death to occur at home; (3) for the
recruited. Physicians’ names and affiliations were obtained sake of ‘‘saving face,’’ patients and their families do not want
from the website of the Society, and questionnaires were death to occur at home; (4) certain family members are expected
distributed by mail with 2 reminders (a total of three). No to care for the patient; and (5) patients ask someone who is not
reward was provided. their relative (eg, friend or neighbor) to take care of them instead
In Korea, due to the lack of a nationwide registry of of their family.
palliative care physicians, questionnaires were distributed via Circumstances surrounding death were examined using 4
3 methods. One was 5-spot surveys at academic congresses or items: (1) patients want a religious person to visit them during
symposiums related to palliative medicine from October 2013 their terminal phase; (2) when the patient dies, family members,
to January 2014, and a total of 97 responses were obtained. The including men, do not hesitate to express emotions (eg, crying
second was an e-mail survey, and a total of 32 responses were out); (3) family members clean the dead body of the patient
obtained from a convenient sample of 110 palliative care themselves; and (4) family members bathe the patient after
physicians through a local network. The third was an additional death. The last 2 were excluded in the Korean questionnaire
hospital-based survey involving palliative care physicians because a pilot test revealed that these questions made no sense
working at 3 hospitals, and 82 responses were obtained. A to Korean participants.
small monetary reward was given for each response.
In Taiwan, all 578 palliative care physicians certified by
Statistical Analyses
the Taiwan Academy of Hospice Palliative Medicine before
June 2012 were recruited. Physicians’ e-mail addresses were To explore the frequencies of physician experience, we
obtained from the Academy, and questionnaires were distrib- adopted 2 comparison methods. One was the analysis of var-
uted via e-mail with 2 reminders (a total of three). A small iance (ANOVA) among the 3 countries; and another was
reward was given to each participant completing the survey. comparing the frequencies of often or very often using Chi-
In all countries, responses to the questionnaire were square tests. Both analyses obtained the same results, so we
voluntary, and confidentiality was maintained throughout all decided to provide the results of the latter, that is, frequencies of
investigations and analyses. No identification numbers were the respondents who answered often or very often, for easier
linked with the original data. The ethical and scientific validity interpretation. We calculated 95% confidence intervals, and a P-
were approved by institutional review boards in each country. value less than 0.01 was regarded as significant.
Specialty was categorized as internal medicine (general
internal medicine, subspecialties of internal medicine, psycho-
Measurements somatic medicine, and family practice), surgery (surgery and
For measurement outcomes, we decided to explore 4 areas: related subspecialties, such as gynecology and otorhinolaryn-
(1) reluctance to take part in end-of-life discussions, (2) role of gology), anesthesiology (anesthesiology, pain medicine), and
family members, (3) home death, and (4) circumstances sur- oncology (medical oncology, radiation oncology, and clinical
rounding death. These measurement outcomes were developed oncology).
based on a systematic literature review regarding this topic,1–22 All analyses were performed using the Statistical Package
discussion among research groups, and preliminary in-depth for the Social Sciences (ver. 11.0) (Chicago, IL).
2 | www.md-journal.com Copyright # 2015 Wolters Kluwer Health, Inc. All rights reserved.
Medicine Volume 94, Number 39, October 2015 Cross-Cultural Study in East Asia
FIGURE 1. Reluctance about end-of-life discussions. P < 0.01; FIGURE 2. Role of family members. P < 0.01; bars demonstrate
bars demonstrate 95% confidence intervals. 95% confidence intervals.
Copyright # 2015 Wolters Kluwer Health, Inc. All rights reserved. www.md-journal.com | 3
Cheng et al Medicine Volume 94, Number 39, October 2015
DISCUSSION
This is the first cross-cultural study investigating common
beliefs and practices when death is approaching in East Asian
countries. The clinical implication for a worldwide audience is
that this study clarified some important points every clinician
should pay attention to in caring for dying patients, from the
East Asian perspective. The research implication is that the
items investigated in this study can be used in further inter-
national surveys of other ethnic populations. Through more
studies on multicultural populations worldwide, we can gain
insight into what is usual in terms of beliefs and practices when
people die.
This study revealed that Confucianism has a strong influ-
ence on behaviors when people die in Korea and Taiwan, but not
in Japan. Confucian philosophy emphasizes family values and
respect for the oldest person. Filial piety is a virtue of respect for
FIGURE 3. Home death. P < 0.01; bars demonstrate 95% con- parents, and is central to Confucian role ethics.4 In an end-of-
fidence intervals. life context, filial piety means to take care of the parents and do
everything good for the parents. In this study, all items inves-
tigating family roles were rated higher in Korea and Taiwan,
that is, physicians give bad news to the oldest or head of the
soul would not be able to return from the hospital; while less family first, all family members are present at the last moment,
than 5% in the other countries had a similar experience and sons/daughters want to do everything they can to esteem
(Figure 3). There were no marked differences among the filial piety. In Korea and Taiwan, dying and death is perceived
countries in the remaining items: less than 15% of physicians not as a personal issue, but rather as a family issue. This study
in all 3 countries stated they often or very often experienced suggests that the Japanese situation seems to be a little different,
‘‘death at home brings bad luck’’ and ‘‘saving face’’ as reasons consistent with some observations.4,20 Japan is moving to put
to avoid home death. In all countries, more than 70% of the more focus on the individual in the modern period, and the role
physicians reported they often or very often found that certain of the family is not as pronounced as in other East Asian
family members were expected to care for the patient at home, countries.
but 10% or less found that friends and neighbors were expected The role of religion is a focus in cross-cultural studies. This
to help in this regard. study highlights the lack of participation of religious persons in
the dying process in Japan, in contrast to Korea and Taiwan.
Circumstance Surrounding Death Japanese generally identify themselves as Buddhist and Shinto,
At the time of death, a smaller number of Japanese but many do not actively participate in religious activities.4 In
physicians than Korean or Taiwanese reported that they often contrast, 40% of Koreans identifies themselves as Buddhists or
or very often experienced patients wanted a religious person to Christians; Korea is an Asian country with a large Christian
visit and family members did not hesitate to express emotions population. Many Taiwanese identify themselves as Buddhist
(crying out). On the other hand, about 40% of the Japanese and Taoist, and frequently visit temples to pray as a part of daily
physicians reported that they often or very often experienced life.4 This finding is in contrast to the situation in Japan, where
family members cleaned the dead body of the patient by palliative care clinicians regard religion as less important for a
themselves (Figure 4). good death, and there are difficulties in obtaining a clear
consensus about what spiritual care is and how spiritual care
should be provided in Japan.22 Moreover, in this survey,
Japanese family members were reported to be less expressive
of emotions at the time of death, as they believe silence is a
preferable attitude at sad events. This finding is in contrast with
the Korean and Taiwanese attitude, in which honestly revealed
emotion is an expression of respect for the deceased.4,25 Clin-
icians should note that the extent to which family members
express emotion at the time of death depends on the cultural
norms of the society and varies culture to culture.
In addition to the effects of Confucianism, each country
has cultural issues unique to that country. In Taiwan, people
want to die at home because they believe the soul would not be
able to return from the hospital if the patient dies in the hospital.
This belief leads to a phenomenon of discharge just before
death: Taiwanese sometimes go back home just before death
even if the patient is unconscious, and this is legal in Taiwan.4
An international meta-analysis revealed factors associated with
death at home, but such beliefs were not investigated.26 This
finding suggests that, in some countries, death at home is not a
FIGURE 4. Circumstances surrounding death. P < 0.01; bars medical issue alone, but rather a cultural one. Also, cleaning the
demonstrate 95% confidence intervals. dead body of the patient by family members themselves is a
4 | www.md-journal.com Copyright # 2015 Wolters Kluwer Health, Inc. All rights reserved.
Medicine Volume 94, Number 39, October 2015 Cross-Cultural Study in East Asia
Japanese tradition. Domestic nationwide surveys revealed that MD (Department of Family Medicine, National Taiwan Uni-
some inpatient hospices in Japan include bathing the patient versity Hospital) for the help in data collection and guidance in
after death as part of their usual care, but 40% of families this study. Taro Nishiura, Med (Division of Clinical Psychology,
cleaned the dead body of the patient by themselves.27,28 Kyoto University), and Sayako Takahashi, Ph.D. (Division of
With regard to traditional reasons to avoid home death, that Clinical Psychology, Kyoto University) for the help in data
is, ‘‘death at home brings bad luck’’ and ‘‘saving face,’’ there management, translation, and technical assistance in this study.
were no marked differences among the three countries. Also, We thank the Japanese Hospice Foundation for the
there were no differences in who were the expected caregivers financial support.
at home: in these 3 countries, those expected to be caregivers at
home were the family; friends, or neighbors were rarely REFERENCES
expected to be informal caregivers at home. Although saving
1. Kagawa-Singer M, Blackhall LJ. Negotiating cross-cultural issues at
face or sekentei has been listed as main reason families in Japan the end of life. JAMA. 2001;286:2993–3001.
do not have professional caregivers,4 we found this value is
2. Searight HR, Gafford J. Cultural diversity at the end of life: issues
consistent in the East Asian countries investigated. Unlike some
and guidelines for family physicians. Am Fam Physician.
countries, such as in Latin America, where friends or neighbors
2005;71:515–522.
are acknowledged as informal caregivers at home, the East
Asian situation puts a strong emphasis on family.1,2,4 3. Gysels M, Evans N, Meñaca A, et al. Culture is a priority for
Reluctance to participate in end-of-life discussions is a research in end-of-life care in Europe: A research agenda. J Pain
Symptom Manage. 2012;44:285–294.
common practice all over the world, especially in Asia.4 The
most hypothesized interpretation is that Confucianism does not 4. Glass AP, Chen LK, Hwang E, et al. A cross-cultural comparison of
systemically refer to life after death, and death has been a taboo hospice development in Japan, South Korea, and Taiwan. J Cross
for long periods.4 This study examined 2 specific reasons for the Cult Gerontol. 2010;25:1–19.
unwillingness to take part in end-of-life discussions, that is, 5. Blackhall LJ, Murphy ST, Frank G, et al. Ethnicity and attitudes
‘‘bad things happen after you say them out loud’’ and ‘‘a bad toward patient autonomy. JAMA. 1995;274:820–825.
life is better than a good death.’’ These are traditional views, 6. Mystakidou K, Parpa E, Tsilila E, et al. Cancer information
especially frequently observed in Taiwan, and more frequently disclosure in different cultural contexts. Support Care Cancer.
in Taiwan than in Korea and Japan. Taiwan is the first county to 2004;12:147–154.
enact a Natural Death Act,20–22 but palliative care clinicians in 7. Bruera E, Neumann CM, Mazzocato C, et al. Attitudes and beliefs
this study reported they experienced more reluctance among of palliative care physicians regarding communication with termin-
patients and families in Taiwan to discuss end-of-life issues than ally ill cancer patients. Palliat Med. 2000;14:287–298.
in Korea and Japan. This might lead to professional and ethical 8. Kwak J, Haley WE. Current research findings on end-of-life decision
conflicts or dilemmas among Taiwanese healthcare pro- making among racially or ethnically diverse groups. Gerontologist.
fessionals,20–22 and further follow-up study on changes in 2005;45:634–641.
public attitudes about end-of-life discussions in East Asia 9. Raijmakers NJH, van Zuylen L, Costantini M, et al. Artificial
is needed. nutrition and hydration in the last week of life in cancer patients. A
This study has several limitations. First, the response rate systematic literature review of practices and effects. Ann Oncol.
in Taiwan was low, and, in Korea, there was no registry of the 2011;22:1478–1486.
subjects to be studied. Recruitment process including payment 10. Chen CH, Tang ST, Chen CH. Meta-analysis of cultural differences
was also different among the countries. Therefore, there may be in western and Asian patients-perceived barriers to managing cancer
a considerable nonresponse and selection bias. Second, the pain. Palliat Med. 2011;26:206–221.
measurement instruments were not formally validated. Never-
11. Yaguchi A, Truog RD, Curtis JR, et al. International differences in
theless, we believe that this is an acceptable limitation, because
end-of-life attitudes in the intensive care unit. Arch Intern Med.
there are no standardized measurement tools for our study aims 2005;165:1970–1975.
and the results obtained in the study are highly interpretable.
12. Cuttini M, Nadai M, Kaminski M, et al. End-of-life decisions in
Third, this study investigated physicians’ views only, which
neonatal intensive care: physicians’ self-reported practices in seven
might be different from actual observations of patients and
European countries. Lancet. 2000;355:2112–2118.
families. Future studies should include direct observation of the
behaviors of patients and families when death is approaching. 13. Chiu TY, Hu WY, Huang HL, et al. Prevailing ethical dilemmas in
Finally, this study did not explore the potential influences if terminal care for patients with cancer in Taiwan. J Clin Oncol.
2009;27:3964–3968.
sociodemographic factors such as education and economic
status and outcomes were measured. This might be addressed 14. Hu WY, Huang CH, Chiu TY, et al. Factors that influence the
in future studies. participation of healthcare professionals in advance care planning for
In conclusion, there are significant intercountry differ- patients with terminal cancer: a nationwide survey in Taiwan. Soc
ences in beliefs and behaviors when death is approaching in Sci Med. 2010;70:1701–1704.
East Asia. Palliative care should be provided in a culturally 15. Cheng SY, Dy S, Hu WY, et al. Factors affecting the improvement
acceptable manner for each country. Future studies on direct of quality of dying of terminally ill patients with cancer through
observations of patients and families are needed. palliative care: a ten-year experience. J Palliat Med. 2012;15:854–
862.
16. Mo HN, Shin DW, Woo JH, et al. Is patient autonomy a critical
ACKNOWLEDGMENTS determinant of quality of life in Korea? End-of-life decision making
We thank Ching-Yu Chen, MD (Department of Family from the perspective of the patient. Palliate Med. 2011;26:222–231.
Medicine, College of Medicine & Hospital, National Taiwan 17. Yun YH, Lee CG, Kim SY, et al. The attitudes of cancer patients
University), Chien-An Yao, MD (Department of Family Medi- and their families toward the disclosure of terminal illness. J Clin
cine, National Taiwan University Hospital), Jaw-Shiun Tsai, Oncol. 2004;22:307–314.
Copyright # 2015 Wolters Kluwer Health, Inc. All rights reserved. www.md-journal.com | 5
Cheng et al Medicine Volume 94, Number 39, October 2015
18. Yun YH, Lee MK, Kim SY, et al. Impact of awareness of terminal 24. Cheng SY, Dy S, Huang SB, et al. Comparison of proxy ratings
illness and use of palliative care or intensive care unit on the of main family caregivers and physicians on the quality of dying
survival of terminal ill patients with cancer: prospective cohort of terminally ill cancer patients. Jpn J Clin Oncol. 2013;43:
study. J Clin Oncol. 2011;29:2474–2480. 795–804.
19. Ruhnke GW, Wilson SR, Akamatsu T, et al. Ethical decision making 25. Hendriks MC, Croon MA, Vingerhoets AJ. Social reactions to adult
and patient autonomy: a comparison of physicians and patients in crying: the help-soliciting function of tears. J Soc Psychol.
Japan and the United States. Chest. 2000;118:1172–1182. 2008;148:22–41.
20. Asai A, Fukuhara S, Lo B. Attitudes of Japanese and Japanese-American 26. Gomes B, Higginson IJ. Factors influencing death at home in
physicians towards life-sustaining treatment. Lancet. 1995;346:356–359. terminally ill patients with cancer: systematic review. BMJ.
21. Matsumura S, Bito S, Liu H, et al. Acculturation of attitudes toward 2006;332:515–521.
end-of-life care: a cross-cultural survey of Japanese Americans and 27. Shinjo T, Morita T, Miyashita M, et al. Care for the bodies of
Japanese. J Gen Intern Med. 2002;17:531–539. deceased cancer inpatients in Japanese palliative care units. J Palliat
22. Murata H, Morita T. Japanese Force Task. Conceptualization of Med. 2010;13:27–31.
psycho-existential suffering by the Japanese Task Force: the first 28. Yamawaki M, Morita T, Kiyohara E, et al. Experience and
step of a nationwide project. Palliat Support Care. 2006;4:279–285. evaluation of caring the body of deceased patient together with
23. Teno JM. Measuring end-of-life care outcomes retrospectively. J nurses: a view from bereaved families. Palliat Care Res.
Palliat Med. 2005;8(Suppl 1):S42–S49. 2015;10:101–107.
6 | www.md-journal.com Copyright # 2015 Wolters Kluwer Health, Inc. All rights reserved.
Original Article
BACKGROUND: A significant share of the cost of cancer care is concentrated in the end-of-life period. Although quality measures of
aggressive treatment may guide optimal care during this timeframe, little is known about whether these metrics affect costs of care.
METHODS: This study used population data to identify a cohort of patients who died of cancer in Ontario, Canada (2005-2009). Indi-
viduals were categorized as having received or having not received aggressive end-of-life care according to quality measures related
to acute institutional care or chemotherapy administration in the end-of-life period. Costs (2009 Canadian dollars) were collected
over the last month of life through the linkage of health system administrative databases. Multivariate quantile regression was used
to identify predictors of increased costs. RESULTS: Among 107,253 patients, the mean per-patient cost over the final month was
$18,131 for patients receiving aggressive care and $12,678 for patients receiving nonaggressive care (P <.0001). Patients who received
chemotherapy in the last 2 weeks of life also sustained higher costs than those who did not (P <.0001). For individuals receiving end-
of-life care in the highest cost quintile, early and repeated palliative care consultation was associated with reduced mean per-patient
costs. In a multivariate analysis, chemotherapy in the 2 weeks of life remained predictive of increased costs (median increase, $536;
P <.0001), whereas access to palliation remained predictive for lower costs (median decrease, $418; P <.0001). CONCLUSIONS: Can-
cer patients who receive aggressive end-of-life care incur 43% higher costs than those managed nonaggressively. Palliative consulta-
tion may partially offset these costs and offer resultant savings. Cancer 2015;121:3307-15. V C 2015 The Authors. Cancer published by
Wiley Periodicals, Inc. on behalf of American Cancer Society. This is an open access article under the terms of the Creative Commons
Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is prop-
erly cited, the use is non-commercial and no modifications or adaptations are made.
INTRODUCTION
The economic burden of cancer is high for both individuals and society as a whole. In 2009, the National Institutes of
Health estimated the annual costs of cancer to have reached 216.6 billion dollars, with 86.6 billion dollars representing
direct medical costs of cancer care.1 Because of the changing incidence, prevalence, and outcomes of malignant diseases,
the financial consequences are anticipated to increase further.2 In particular, a disproportionate share of health care costs is
concentrated in the end-of-life period.2-4 Prior research in the United States and Canada has established quality measures
of aggressive management for the last months of life.5-9 High rates of unplanned medical encounters such as emergency
room visits, hospitalizations, and intensive care stays, for example, may indicate inattention to symptomatic issues, a lack
of advance directives, or inadequate utilization of home and hospice services. Chemotherapy administered in the last days
of life may offer little chance of clinical benefit but notable consequences, including toxicities that impair quality of life
and delay access to hospice care.10,11 Although quality measures of aggressive management may signal suboptimal oncol-
ogy care, little is known about whether quality-based end-of-life care can result in cost savings.
Implicit in the assumption that aggressive care is suboptimal at the end of life is the suggestion that a palliative focus
could improve the quality of care. When physicians simply engage in end-of-life conversations, their patients experience
less aggressive medical care near death (including fewer intensive care unit [ICU] admissions) with improved quality of
life.12,13 With additional consultation with palliative care teams, further benefits in patient satisfaction and health care
Corresponding author: Matthew C. Cheung, MD, SM, Odette Cancer Centre, Sunnybrook Health Sciences Centre, 2075 Bayview Avenue, T2-031, Toronto,
Ontario, Canada M4N3M5; Fax: (416) 480-6002; matthew.cheung@sunnybrook.ca
1
Odette Cancer Centre, Sunnybrook Health Sciences Centre and University of Toronto, Toronto, Canada; 2Ontario Institute for Cancer Research, Toronto, Canada;
3
Institute for Clinical Evaluative Sciences, Toronto, Canada; 4Health Outcomes and Pharmacoeconomic Research Centre, Sunnybrook Research Institute,
Sunnybrook Health Sciences Centre, Toronto, Canada; 5Canadian Centre for Applied Research in Cancer Control, Toronto, Canada; 6Department of Pharmacology,
University of Toronto, Toronto, Canada; 7International Centre for Health Innovation, Richard Ivey Business School, Western University, London, Canada.
Additional Supporting Information may be found in the online version of this article.
DOI: 10.1002/cncr.29485, Received: March 17, 2015; Revised: April 22, 2015; Accepted: April 24, 2015, Published online May 29, 2015 in Wiley Online Library
(wileyonlinelibrary.com)
Database Description
Ontario Cancer Registry Population-based database with approximately 95% of all provincial cancer
diagnoses captured
Ontario Health Insurance Plan Contains all billing claims for physician services and certain other health
professionals (including fee codes for chemotherapy administration)
Canadian Institute for Health Information Discharge Abstract Database Contains demographic, administrative, and clinical data related to hospital
admissions (including the provision of intensive care unit care)
National Ambulatory Care Reporting System Contains information on ambulatory care visits (including emergency depart-
ment care)
Home Care Database Contains information on government-funded care at home
Registered Persons Database Contains basic demographics and dates of death for all Ontario residents el-
igible for Ontario Health Insurance coverage
utilization have been demonstrated.14,15 As such, it would days of death. This study was approved by the Research
be anticipated that palliation could reduce the use of Ethics Board at Sunnybrook Health Sciences Centre.
costly resources. Supporting this contention, preliminary
research has suggested that end-of-life discussions16 and Cohort Selection and Variable Definitions
conversations about spirituality17 might reduce costs of Patients with cancer as the cause of death were identified
care. Conversely, palliative consultation and placements in the Ontario Cancer Registry.19 International Classifica-
have their own intrinsic costs. The relation between pallia- tion of Diseases, Ninth Revision (ICD9) codes were used to
tive care, aggressiveness of care, and costs warrants further identify the type of cancer death (breast [ICD9-174],
evaluation. lung [ICD9-162], colorectal [ICD9-153 and ICD9-154],
We used population-level administrative databases prostate [ICD9-185], hematologic [ICD9-196 and
to identify the costs of end-of-life care in patients man- ICD9-200 to ICD9-208], and other [all other ICD9 can-
aged with aggressive and nonaggressive intent on the basis cer codes]). As previously described, patient cases from
of previously established quality measures. Distinctly from the Ontario Cancer Registry were linked to administrative
the aggressiveness of care received, we further assessed the databases (Table 1) with encrypted insurance numbers to
impact of preceding palliative care services on costs of determine whether quality measures were performed.5
care. We hypothesized that patients receiving aggressive The neighborhood income quintile was assigned by
care near the end-of-life would use more resources and the linkage of the patient’s postal code (from the Regis-
correspondingly incur greater costs of care in comparison tered Persons Database) to the median income by dissemi-
with individuals who did not receive aggressive care. nation area identified from the Statistics Canada 2006
census. The rural status (communities with a population
size < 10,000) and the regional designation in Ontario
MATERIALS AND METHODS (based on the local health integration networks) were
Study Design based on the city, postal code, and dissemination area of
We used public administrative databases to identify the patient’s residence. Patient comorbidity was calculated
resources and costs associated with end-of-life cancer care with the Deyo adaptation20 of the Charlson comorbidity
for adult patients in Ontario, Canada who died between index measure21 according to inpatient diagnoses in the
January 1, 2005 and December 31, 2009. We excluded last 2 years of life.
cases if they did not have a valid provincial health insur- Palliative care was defined by hospitalization, home
ance number, died within 30 days of the initial cancer di- care, or physician billing codes specific for palliative con-
agnosis, or were younger than 20 years. Individuals in the sultation (see online supporting information). To identify
decedent cohort were categorized as having received or patients who had received repeated and earlier palliative
having not received aggressive end-of-life management care services before the final days of life, we defined
according to the following quality measures5,7,18: 1) patients as palliative if at least 2 palliative care codes were
chemotherapy administered within 14 days of death, 2) identified at least 30 days apart and in the last 365 days
more than 1 emergency department (ED) visit within 30 before death. The palliative care designation was a unique
days of death, 3) more than 1 hospitalization within 30 predictor variable mutually distinct from the aggressive
days of death, or 4) at least 1 ICU admission within 30 quality measures.
Abbreviations: ED, emergency department; ICU, intensive care unit; LHIN, local health integration network; SD, standard deviation.
Figure 1. Trends in aggressive end-of-life care in Ontario according to the palliative designation (% of cohort on y-axis): (A) >1
ED visit in the last 30 days of life, (B) chemotherapy in the last 14 days of life, (C) intensive care unit admissions in the last 30
days of life, and (D) hospitalizations in the last 30 days of life. ED indicates emergency department.
differential between aggressive and nonaggressive end-of- cohort for the study. Table 2 presents demographic char-
life care. Analyses were further stratified according to the acteristics of patients who did and did not receive aggres-
palliative designation. Multivariate quantile regression sive care. In the cohort, 24,095 patients (22.5%)
analysis was used to estimate effects of the palliative desig- experienced at least 1 quality measure of aggressive end-
nation and the aggressive quality measures on median of-life care.
costs. In quantile regression, the quantiles or percentiles During the study period, 3.6% of the cohort
of the distribution of costs are modeled as a function of received systemic chemotherapy in the last 2 weeks of life.
predictor characteristics.22 Because mean costs are poten- The remaining indicators were noted more frequently:
tially more susceptible to outliers than median costs,23 we 14.7% experienced more than 1 ED visit in the last 30
felt that this modeling was a more appropriate method to days of life, 6.3% of patients experienced multiple hospi-
avoid overestimating the impact of the aggressive indicators talizations in the final month of life, and 5.5% experi-
on overall end-of-life costs. Models were adjusted for the enced ICU admissions in the final month of life. Figure 1
age at death (continuous variable centered on the age of 20 depicts the trends in aggressive management for each indi-
years), sex, cancer type (hematologic vs nonhematologic), cator over the study time horizon stratified by the pallia-
income quintile, Charlson score, duration of disease, resi- tive designation. At all time points, patients who were
dence (urban vs rural), and year of death (continuous vari- designated as palliative were less likely to receive aggressive
able centered on the year 2005). All analyses were care according to all 4 quality measures.
performed with SAS 9.1.3 (SAS Institute, Cary, NC).
Costs of Care
RESULTS The mean cost per patient in the last month of life was
Baseline Characteristics and Aggressive $13,903 Canadian dollars (median, $10,859; interquar-
Care Indicators tile range [IQR], $5387-$18,498). The predominant cost
There were 107,253 patients who died of cancer in On- driver during this period was hospitalizations (contribut-
tario, Canada and met our inclusion criteria to form the ing 64.7% of the total cost), with a mean cost of $8998.
Nonaggressive Aggressive
Care Care
Abbreviation: NDFP, New Drug Funding Program. Figure 2. Effect of the palliative designation according to
Disaggregated costs may not add up to the total amount because of quintiles of end-of-life costs (in Canadian dollars) stratified
rounding. Data are presented as means and standard deviations. by patients receiving aggressive care and patients receiving
a
Other costs include admissions for mental health, dialysis, rehabilitation, nonaggressive care.
and devices.
Table 3 lists the overall mean costs and disaggre- In the overall cohort, 69,715 patients (65.0%) were
gated costs for patients who received aggressive care and designated as palliative on the basis of system billing codes
patients who did not. The mean per-patient costs over the associated with the provision of palliative services. For
final month were $18,131 (median, $14,464; IQR, patients ultimately managed aggressively and patients
$9437-$21,658) for patients receiving aggressive care and managed nonaggressively, the proportions of patients ini-
$12,678 (median, $9586; IQR, $4456-$17,414) for tially designated as palliative were 54.1% and 68.2%,
patients receiving nonaggressive care; the difference was respectively. Palliative patients incurred lower mean costs
$5453 (P < .0001). For individuals with 1 (n 5 16,867), (mean, $13,503 vs $14,644) but higher median costs
2 (n 5 6220), 3 (n 5 946), or all 4 indicators of care (median, $10,988 vs $10,573) in comparison with
(n 5 62), the mean per-patient costs increased to patients who were not palliative. We further analyzed the
$17,001, $20,304, $23,690, and $22,700, respectively. relation of the palliative designation with quintiles of
Aggressive care patients incurred higher costs for hos- costs. For individuals receiving end-of-life care in the
pitalization, ED visits, and physician services in highest cost quintiles (the top 2 quintiles), palliative care
comparison with nonaggressive care patients. In contrast, consultation was associated with reduced mean per-
nonaggressive care was associated with higher costs for patient costs. However, for individuals receiving end-of-
the provision of complex continuing care (including inpa- life care in the lowest cost quintiles (the bottom 2 quin-
tient palliation) and home care. Hospitalizations remained tiles), palliation was associated with increased per-patient
the key cost drivers for patients managed both aggressively costs. This relation between palliative care and costs was
and nonaggressively ($12,541 and $7971, respectively). seen in patients who were managed either aggressively or
We separately compared costs for individuals who nonaggressively. The most significant reduction in mean
received systemic chemotherapy in the last 14 days of life per-patient costs associated with the palliative designation
as the sole indicator of aggressive care. The mean per- occurred in aggressively managed patients in the highest
patient costs over the final month were $16,110 (median, cost quintile (Fig. 2).
$12,433; IQR, $8045-$19,599) for patients receiving Multivariate quantile regression models were con-
chemotherapy and $13,820 (median, $10,794; IQR, structed to study the effects of the palliative designation,
$5269-$18,454) for patients who did not receive treatment aggressive care indicators, and patient variables on median
(P < .0001). Patients treated with chemotherapy in the 2 end-of-life costs (Table 4). In the initial model including
weeks before death incurred higher hospitalization, ED, the palliative designation, individuals were more likely to
physician-related, and chemotherapy drug costs, whereas have high end-of-life expenditures if they were younger,
those who did not receive this treatment incurred higher were female, were in the lowest income quintile, had been
palliative care and home care costs (data not shown). diagnosed with a hematologic malignancy, were affected
Parameter Level Estimate (SE) P Estimate (SE) P Estimate (SE) P Estimate (SE) P Estimate (SE) P
Intercept 6562.99 (187.96) <.0001 5991.87 (185.15) <.0001 6509.6 (182.62) <.0001 5902.1 (186.42) <.0001 5651.37 (178.96) <.0001
Agea 264.22 (2.5) <.0001 258.71 (2.44) <.0001 263.41 (2.44) <.0001 255.87 (2.51) <.0001 252.93 (2.4) <.0001
b
Sex Male — .0447 — .0005 — .0287 — .0068 — .0006
Female 122.3 (60.93) 192.53 (55.19) 127.66 (58.36) 165.58 (61.22) 193.8 (56.57)
Year of deathc 540.35 (21.86) <.0001 523.55 (20.29) <.0001 540.42 (20.81) <.0001 515.36 (21.97) <.0001 544.43 (20.33) <.0001
Income quintile Highestb — .1696 — .2253 — .1703 — — .342
Second highest 135.62 (98.73) .0389 108.37 (89.37) .0587 131.39 (95.82) .0484 146.82 (99.31) .1393 87.44 (92.02) .1345
Middle 204.26 (98.88) .0864 153.43 (81.17) .4671 188.09 (95.28) .0863 201.37 (94.83) .0337 130.92 (87.48) .3506
Second lowest 159.61 (93.09) .0002 61.44 (84.48) .0006 149.36 (87.07) .0002 168.57 (91.51) .0655 79.54 (85.22) .0004
Lowest 368.81 (98.97) 297.01 (86.49) 365.75 (96.94) 404.14 (97.7) <.0001 311.04 (87.31)
Rurality Ruralb — .5717 — .0093 — .6169 — .5622 — .0027
Urban 47.67 (84.28) 214.26 (82.34) 41.65 (83.26) 48.47 (83.63) 236.68 (78.96)
Cancer type Nonhematologicb — <.0001 — <.0001 — <.0001 — <.0001 — <.0001
Hematologic 3749.67 (152.93) 3554.97 (161.81) 3728.2 (151.04) 3054.94 (156.95) 3333.51 (159.66)
Duration of cancer — <.0001 — <.0001 — <.0001 — <.0001 — <.0001
223.94 (4.83) 225.74 (2.7) 223.59 (4.05) 226.31 (4.97) 224.82 (3.6)
Charlson score 0b — — — — —
1 1543.29 (192.49) <.0001 1436.88 (166.97) <.0001 1550.24 (193.89) <.0001 1443.00 (169.11) <.0001 1525.72 (175.7) <.0001
2 7045.36 (58.42) <.0001 6609.97 (54.34) <.0001 7039.43 (55.24) <.0001 6697.68 (60.63) <.0001 6517.95 (56.61) <.0001
Palliative designation Nob — <.0001 — <.0001 — <.0001 — .6155 —
Yes 2423.29 (65.45) 2236.50 (60.14) 2418.26 (62.21) 233.21 (66.11) 2221.14 (61.37) .0003
>1 ED visit Nob — <.0001
Yes 2636.41 (73.15)
Chemotherapy indicator Nob — <.0001
Yes 536.35 (89.26)
ICU indicator Nob — <.0001
Yes 9546.38 (258.61)
>1 hospitalization Nob — <.0001
Yes 6077.94 (102.11)
Abbreviations: ED, emergency department; ICU, intensive care unit; SE, standard error.
Cancer
a
Continuous variable centered on the age of 20 years.
b
Reference group.
c
Continuous variable centered on the year 2005.
by multiple comorbidities, had experienced a shorter du- intrinsic costs required for such care. The palliative desig-
ration of disease, or had died in the later years of the study nation remained predictive for decreased costs in multi-
period (for a model example, see online supporting infor- variate models after adjustments for clinical variables.
mation). The palliative designation independently Notably, the sole model in which the cost savings with
reduced median costs by $423 (P < .0001). In subsequent palliation did not achieve statistical significance (median
models, the impact of the individual quality measures was decrease, $33; P 5 .6155) was the model in which the
studied (models 2-5). In the model that incorporated ICU indicator dramatically increased costs (median
chemotherapy in the last 14 days of life, this aggressive in- increase, $9546; P < .0001). In the remaining analyses,
dicator was independently associated with increased costs the palliative designation continued to independently pre-
(median increase, $536; P < .0001), whereas the palliative dict lower costs. This is in keeping with prior research
designation remained predictive of decreased costs (me- demonstrating less intensive care and resource consump-
dian decrease, $418; P < .0001). tion when earlier palliative care is instituted.14 In random-
ized trials of patients with advanced cancer, patients
DISCUSSION allocated to earlier palliative care reported improved qual-
Quality measures for the end-of-life period were initially ity of life and were less likely to receive aggressive end-of-
derived to determine health care systems that might strug- life care.15,25,26 In an observational study, Zhang et al16
gle in providing appropriate patient-centered care.7 studied the impact of end-of-life conversations between
Although aggressive care may be warranted or requested cancer patients and physicians on costs in the last week of
for individual patients, on a system level, the associated life. Patients who reported discussions about palliation
indicators of such care might denote inadequate prepara- incurred costs of $1876 (2008 US dollars), whereas the
tion or a lack of supportive services for those in the last cost was $2917 for those who did not. We speculate that
days of life.24 These indicators have thus been positioned our palliative designation might serve as a surrogate for
as system measures for poor-quality care. Our results indi- conversations about end-of-life preferences or the avail-
cate that aggressive end-of-life care is more expensive than ability of palliative services and might potentially modu-
nonaggressive care. In the final month of life, the care for late medical expenditures even among those destined to
aggressively managed patients was $5453 more (or 43% receive aggressive care. Further research is needed to
costlier) than nonaggressive care. Aggressively managed define the optimal timing and nature of palliative consul-
patients were more likely to incur higher costs for acute tation to optimize resource utilization and, more impor-
care and physician services, whereas nonaggressively man- tantly, patient outcomes.
aged patients generated higher costs for home care and Our results are in keeping with prior costing efforts
complex continuing care, which included the provision of for cancer patients at the end of life in both public27 and
inpatient palliation. private health care systems.4 In the United States, Chastek
Because 3 of the 4 quality measures were intrinsi- et al4 used claims data to identify cancer-related costs for
cally linked with more expensive resource utilization, 28,530 patients with active cancer 6 months before death.
namely, institutional care, we separately evaluated the They established costs related to inpatient stays, hospice
costs with the chemotherapy indicator as the sole care, and outpatient services of $74,212 (2009 US dollars)
reflection of aggressive end-of-life care. Once again, and identified inpatient care as the key cost driver. This
patients treated aggressively according to this definition analysis focused on a select population of commercially
incurred higher costs than their nonaggressively treated insured individuals and did not stratify outcomes accord-
counterparts. ing to aggressive indicators of care. In contrast, a study
Our study is the first to examine the unique relation from Kyoto, Japan did analyze costs according to select
of a palliative designation with aggressive management aggressive quality measures, albeit in a smaller population
and end-of-life expenditures. We chose a palliative desig- (n 5 3143) of predominantly self-employed, unem-
nation to reflect repeated and earlier access to palliation. ployed, or elderly individuals (with the majority older
For patients destined to receive more costly (and aggres- than 75 years).28 The investigators studied the costs asso-
sive) care, we found that earlier access to palliative consul- ciated with the last 3 months of life but exclusively for
tation and services could meaningfully reduce costs. For those who received institutional care. Death in an acute-
patients who would ultimately consume few health care care hospital (rate ratio [RR], 1.32; P < .001) and chemo-
resources (and potentially less aggressive care), palliative therapy in the last month of life (RR, 1.25; P < .001)
care was associated with higher costs, likely because of the were associated with higher end-of-life costs. In contrast
22. Koenker R, Bassett G. Regression quantiles. Econometrica. 1978;46: 28. Morishima T, Lee J, Otsubo T, et al. Association of healthcare
33-50. expenditures with aggressive versus palliative care for cancer patients
23. Austin PC, Ghali WA, Tu JV. A comparison of several regression at the end of life: a cross-sectional study using claims data in Japan.
models for analysing cost of CABG surgery. Stat Med. 2003;22: Int J Qual Health Care. 2014;26:79-86.
2799-2815. 29. Longo CJ, Deber R, Fitch M, et al. An examination of cancer
24. Earle CC, Landrum MB, Souza JM, et al. Aggressiveness of cancer patients’ monthly ‘out-of-pocket’ costs in Ontario, Canada. Eur J
care near the end of life: is it a quality-of-care issue? J Clin Oncol. Cancer Care (Engl). 2007;16:500-507.
2008;26:3860-3866. 30. Dumont S, Jacobs P, Turcotte V, et al. The trajectory of palliative
25. Temel JS, Greer JA, Muzikansky A, et al. Early palliative care for care costs over the last 5 months of life: a Canadian longitudinal
patients with metastatic non–small-cell lung cancer. N Engl J Med. study. Palliat Med. 2010;24:630-640.
2010;363:733-742. 31. Jacobson M, O’Malley AJ, Earle CC, et al. Does reimbursement
26. Zimmermann C, Swami N, Krzyzanowska M, et al. Early palliative influence chemotherapy treatment for cancer patients? Health Aff
care for patients with advanced cancer: a cluster-randomised con- (Millwood). 2006;25:437-443.
trolled trial. Lancet. 2014;383:1721-1730. 32. Matsuyama R, Reddy S, Smith TJ. Why do patients choose chemo-
27. Walker H, Anderson M, Farahati F, et al. Resource use and costs of therapy near the end of life? A review of the perspective of those fac-
end-of-life/palliative care: Ontario adult cancer patients dying during ing death from cancer. J Clin Oncol. 2006;24:3490-3496.
2002 and 2003. J Palliat Care. 2011;27:79-88.
doi:10.1093/jnci/dju424
First published online January 20, 2015
Article
article
Palliative Care and the Aggressiveness of End-of-Life
Care in Patients With Advanced Pancreatic Cancer
Raymond W. Jang, Monika K. Krzyzanowska, Camilla Zimmermann,
Correspondence to: Raymond W. Jang, Princess Margaret Cancer Centre, 610 University Avenue, Rm 5–217, Toronto, ON M5G 2M9, Canada
(e-mail: raymond.jang@uhn.ca).
Abstract
Background: We examined the impact of palliative care (PC) on aggressiveness of end-of-life care for patients with
advanced pancreatic cancer. Measures of aggressive care included chemotherapy within 14 days of death; and at least one
intensive care unit (ICU) admission, more than one emergency department (ED) visit, and more than one hospitalization, all
within 30 days of death.
Methods: A retrospective population-based cohort study using administrative data was conducted in patients with
advanced pancreatic cancer from 2005 to 2010 in Ontario, Canada. Multivariable logistic regression was performed with
the above measures of aggressive care as the outcomes of interest and PC as the main exposure, adjusting for covariables.
Secondary analyses examined intensity of PC as the main exposure defined in two ways: 1) absolute number of PC visits
before the outcome of interest (0, 1, 2, 3+ visits) and 2) monthly rate of PC visits.
article
Results: The cohort included 5381 patients (median survival 75 days); 2816 (52.3%) had received a PC consultation. PC
consultation was associated with decreased use of chemotherapy near death (odds ratio [OR] = 0.34, 95% confidence
interval [CI] = 0.25 to 0.46); lower risk of ICU admission: OR = 0.12, 95% CI = 0.08 to 0.18; multiple ED visits: OR = 0.19, 95%
CI = 0.16 to 0.23; multiple hospitalizations near death: OR = 0.24, 95% CI = 0.19 to 0.31). A per-unit increase in the monthly
rate of PC visits was associated with lower odds of aggressive care for all four outcomes.
Conclusion: PC consultation and a higher intensity of PC were associated with less aggressive care near death in patients
with advanced pancreatic cancer.
Pancreatic cancer is a common and lethal type of cancer (1). department (ED). In a recent study, patients with pancreatic
Surgery is the only curative treatment, but only around 20% of cancer were second only to those with lung cancer in the fre-
patients are surgical candidates because most have advanced quency of ED visits in both the last six months and the last two
disease at diagnosis. Even among those who have a poten- weeks of life (3).
tially curative surgical resection, the five-year survival is only Given that the majority of patients with pancreatic cancer
20% (2). Patients with pancreatic cancer also have a high bur- die in a short period of time and with a high symptom burden,
den of symptoms and are frequent users of the emergency how they die, their quality of life near death, and the quality
Received: April 18, 2014; Revised: October 13, 2014; Accepted: November 26, 2014
© The Author 2015. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com.
1 of 8
R. W. Jang et al. | 2 of 8
of care that they receive are important. For these reasons, pan- 95% complete (36). Index cases from the OCR were linked using
creatic cancer is a good prototype cancer to study the quality encrypted provincial health card numbers across different data
of care that patients receive near death. Aggressive care near sources. The data sources included: 1) Ontario Health Insurance
death for patients with incurable cancers is an important end- Plan (OHIP) (37) claims database, which contains information on
of-life quality indicator (4,5), as aggressive care has been linked billing claims for physicians’ services provided to Ontario resi-
with worse quality of life for the patient and worse bereavement dents, 2) the Canadian Institute for Health Information (CIHI)
adjustment for their caregivers (6,7). Discharge Abstract Database (DAD) (38), which contains diag-
The most common indicators used to study aggressive nostic and procedure information on all discharges from acute
care near death include the administration of chemotherapy care facilities and information on same-day surgeries, 3) the
near death, frequent ED visits near death, hospitalizations CIHI National Ambulatory Care Reporting System (NACRS) (39),
near death (including death in a hospital), and intensive care which captures information on emergency department visits,
unit (ICU) admissions near death (4,5,8–13). However, quality and 4) the Registered Persons Database (RPDB), which provides
indicators are only useful if they are linkable to interventions basic sociodemographic information.
that can be shown to improve areas of suboptimal perfor-
mance. Because of its patient-centered approach and focus
Cohort Selection
on pain and symptom management (14), palliative care (PC)
may be an ideal intervention to reduce aggressiveness of care The OCR does not contain staging information for pancreatic
near death. cancer. Therefore, in order to avoid the bias of including patients
article
esis was that PC would be associated with decreased aggressive within 30 days of death).
care near death for these patients. A secondary objective was to study the impact of the inten-
sity of PC using the same four measures of aggressive care. The
Methods intensity of PC was defined in two ways: 1) absolute number of
PC visits before the outcome of interest (0, 1, 2, 3+ visits) and
Study Design 2) monthly rate of PC visits defined as: number of PC visits ÷
We conducted a population-based, retrospective study of (survival time in days ÷ 30). Patients who lived less than 14 days
an incident cohort of all patients who were diagnosed with were excluded, as their limited survival would have artificially
advanced pancreatic cancer in Ontario, Canada, between Jan 1, inflated the monthly rate (eg, if a person has one PC visit but
2005 and Dec 31, 2010 and who subsequently died. Follow-up only lived for one day, the monthly rate would be 1/[1/30] = 30
data were available until March 2011. We included only patient visits). The PC visits were counted from the day of diagnosis
cases with a valid provincial health insurance number and until each outcome of interest.
age 18 years or older at the time of diagnosis. Ethics approval The four outcome measures of aggressive end-of-life care
was obtained from the University Health Network and the were based on previous studies (5,41,42) and used the same
University of Toronto. Patient informed consent was waived, as codes as a previous Ontario study (41). PC was defined using
the data was deidentifed and anonymized before given to the OHIP physician billing data. Data sources and definitions of
investigators. important variables are provided in Supplementary Table 1.
We used the Ontario Cancer Registry (OCR) to identify index We calculated the frequency of each of the measures of aggres-
cases of patients with a diagnosis of pancreatic cancer. The sive care for all patients and conducted subset analyses for
OCR is a population-based cancer registry and is approximately those who received or did not receive PC. The denominator
3 of 8 | JNCI J Natl Cancer Inst, 2015, Vol.107, No.3
included all patients who died with a diagnosis of an advanced a propensity score for the likelihood of receiving PC, ranked all
pancreatic cancer. Chi-squared (χ2) tests were performed as the patients, created quintiles based on this score, and included
a first test to determine differences in aggressiveness of care the scores as an independent variable in our four main regres-
among patients who did and did not receive palliative care. All sion analyses.
statistical tests were two-sided and a P value of less than .05 was Lastly, we examined the effect of the medical oncologist on
considered statistically significant. each of our outcomes by using a two-level hierarchical random
Multivariable logistic regression analyses were used to pre- effects model. The specific methodology and results are outlined
dict the likelihood of experiencing each of the outcomes of in the supplemental file.
aggressive care, with PC as the main exposure and the following
variables as covariables: age, sex, rural residence, health region,
year of diagnosis, income quintile, primary care physician Results
involvement, medical oncologist involvement (for outcomes
other than chemotherapy near death), chemotherapy (for out-
Cohort Description and Patient Demographics
comes other than chemotherapy near death), and Charlson-Deyo In our initial cohort, 7928 patients were diagnosed with pancre-
Comorbidity Index Score (0, 1, 2+) (43). The index was obtained atic cancer in Ontario. Of these, 670 were excluded because they
from hospitalizations and same-day surgery admissions only. had a diagnosis of a second cancer, leaving 7258 patients. Of
Similar analyses were performed for the secondary objective, the 7258 patients, 1182 were excluded because they underwent
using the two definitions of intensity of PC in separate models. pancreatic cancer surgery (533 without adjuvant chemotherapy,
death: chemotherapy near death (OR = 0.34, 95% CI = 0.25 to hospitalizations near death (OR = 0.24, 95% CI = 0.19 to 0.31).
0.46); ICU admission (OR = 0.12, 95% CI = 0.08 to 0.18), mul- More frequent PC visits were associated with fewer instances of
tiple ED visits (OR = 0.19, 95% CI = 0.16 to 0.23), and multiple aggressive care, as seen in Table 4.
article
3+ 1748 (32.5%) ity of life for the patient and worse bereavement adjustment for
Survival (all patients) their caregivers (6,7). Despite recent evidence on the benefits
Median (mean) 75 (147) days of PC (31,45), few studies have examined the impact of PC on
Interquartile Range 27–188 days aggressiveness of care near death from a population perspec-
Survival (patients who received palliative chemotherapy) tive. In our cohort of patients with advanced pancreatic cancer,
Median (mean) 199 (264) days a PC consultation was associated with less aggressive care near
Survival by receipt of PC death. This finding was consistent across all four measures of
Median (mean) aggressive care near death (ie, chemotherapy, ICU admissions,
PC 100 (172) days multiple ED visits, and hospitalizations). The magnitude of ben-
No PC 51 (120) days
efit was also large, as all the odds ratios ranged from 0.12 to 0.34
* These patients do not have a calculable Charlson score, because they were not
on multivariable analyses. Furthermore, we found that more
hospitalized or did not have same-day surgery during the two years prior to intensive PC follow-up was associated with fewer instances of
diagnosis to last follow-up. PC = palliative care. aggressive care near death.
Table 2. Unadjusted frequency of each outcome for all patients and by receipt of PC (advanced cohort; n = 5381)*
Outcome All patients, No. (%) PC, No. (%) No PC, No. (%)
Chemotherapy near death 218/5381 (4.1) 73/2790 (2.6) 145/ 2591 (5.6)
ICU near death 234/5381 (4.3) 31/2775 (1.1) 203/2606 (7.8)
Multiple ED visits near death 993/5381 (18.5) 190/2560 (7.4) 803/2821 (28.5)
Multiple hospitalizations near death 447/5381 (8.3) 103/2697 (3.8) 344/2684 (12.8)
* To be considered as having received palliative care (PC), the PC consultation had to occur before the outcome of interest. ED = emergency department; ICU = inten-
sive care unit; PC = palliative care.
5 of 8 | JNCI J Natl Cancer Inst, 2015, Vol.107, No.3
Referent
Referent
Figure 1. Frequency of aggressive care by number of palliative care visits.
ED = emergency department; ICU = intensive care unit.
* Models were also adjusted for health region, but this variable is not shown for ease of presentation. ED = emergency department; ICU = intensive care unit; OR = odds ratio.
Multiple ED visits near death
Multiple sensitivity analyses, including using only the subco-
OR (95% CI)
(hierarchical modelling and propensity score modelling) did not
Referent
Referent
appreciably change our main findings. Specifically, the hierar-
chical random effects model with the medical oncologist as
the clustering variable provides evidence that the results are
not simply because of certain medical oncologists recommend-
ing both a palliative care consultation and less aggressive care
near death.
There are several elements of a palliative care consultation
that could explain its association with decreased aggressiveness
of care. One likely element is that of simply having an end-of-
life conversation, as this has been shown to decrease aggres-
sive care near death (46). A recent qualitative study associated
0.12 (0.08 to 0.18)
with the trial by Temel and colleagues (31) described seven key
OR (95% CI)
Referent
Referent
elements to a PC consultation: relationship and rapport build-
ing, symptom assessment, addressing coping issues, estab-
lishing illness understanding, discussing cancer treatments,
Table 3. Logistic regression analyses predicting aggressive care near death (n = 5381)*
not clear how many visits are necessary, in the study by Temel
Referent
Referent
Year of diagnosis
Income quintile
Charlson index
Chemotherapy
Palliative care
Male sex
Rurality
admitted to the ICU but more likely to have multiple ED visits near
death. These findings likely reflect the lack of certain health care
R. W. Jang et al. | 6 of 8
Chemotherapy near death ICU near death Multiple ED visits near death Multiple hospitalizations near death
Number of PC visits
Ref. 0 Referent Referent Referent Referent
1 0.73 (0.47 to 1.16) 0.25 (0.13 to 0.46) 0.36 (0.27 to 0.48) 0.47 (0.33 to 0.69)
2 0.26 (0.14 to 0.51) 0.13 (0.06 to 0.29) 0.29 (0.22 to 0.40) 0.44 (0.30 to 0.64)
3+ 0.26 (0.17 to 0.38) 0.09 (0.05 to 0.16) 0.11 (0.09 to 0.15) 0.12 (0.09 to 0.18)
Monthly rate of PC
visits, visits/month
Ref. 0 Referent Referent Referent Referent
1 0.69 (0.58 to 0.81) 0.31 (0.21 to 0.46) 0.31 (0.26 to 0.38) 0.31 (0.24 to 0.40)
* Patients who lived less than 14 days were excluded, as their limited survival would have artificially inflated the monthly rate (eg, if a person has one palliative care visit
but only lived for one day, the monthly rate would be 1/[1/30] = 30 visits). ED = emergency department; ICU = intensive care unit; OR = odds ratio; PC = palliative care.
Table 5. Sensitivity analysis: comparison of the effect of palliative care using different models
Adjusted odds ratio of the effect of palliative care on the specified outcome (95% CI)
Chemotherapy
near death
Ref. No PC Referent Referent Referent Referent Referent Referent
PC 0.34 (0.25 to 0.46) 0.22 (0.16 to 0.30) 0.30 (0.22 to 0.43) 0.34 (0.25 to 0.47) 0.29 (0.21 to 0.39) 0.35 (0.26 to 0.48)
ICU near death
Ref. No PC Referent Referent Referent Referent Referent Referent
PC 0.12 (0.08 to 0.18) 0.21 (0.11 to 0.39) 0.13 (0.08 to 0.19) 0.12 (0.08 to 0.18) 0.15 (0.10 to 0.25) 0.13 (0.09 to 0.19)
Multiple ED visits
near death
Ref. No PC Referent Referent Referent Referent Referent Referent
PC 0.19 (0.16 to 0.23) 0.36 (0.28 to 0.48) 0.19 (0.16 to 0.23) 0.20 (0.17 to 0.24) 0.22 (0.18 to 0.27) 0.20 (0.17 to 0.24)
Multiple hospitalizations
near death
Ref. No PC Referent Referent Referent Referent Referent Referent
PC 0.24 (0.19 to 0.31) 0.24 (0.19 to 0.31) 0.24 (0.19 to 0.31) 0.25 (0.20 to 0.32) 0.29 (0.22 to 0.38) 0.25 (0.20 to 0.32)
article
* The survival duration covariable was a categorical variable: short (<90 days), medium (≥90 days and < 180 days), and long (≥180 days).
† For the random effects model, the n of 3393 is smaller than the overall n of 5381 because only approximately 60% of patients saw a medical oncologist, and
the clustering is around individual medical oncologists. The binary covariable of medical oncologist (TRUE/FALSE) was excluded. ED = emergency department;
ICU = intensive care unit; PC = palliative care.
resources available in rural areas. At a more general level, these Other limitations of our study include the fact that admin-
findings suggest that the different measures of aggressive care istrative databases are neither 100% complete or accurate, the
measure different aspects of such care, and that, at least for some unavailability of variables such as patient performance status
measures of aggressiveness, the input variables go beyond that of and symptom burden, and the lack of validation of certain billing
a physician and the patient and family. codes. Case ascertainment bias may exist, as not all patients would
Our study has several limitations. As a way to overcome the have had pathologic confirmation of the diagnosis. Selection bias
biases and limitations inherent with observational studies, we exists in how we defined the final cohort. In our goal of exclud-
performed multiple sensitivity analyses. However, we cannot ing patients with potentially curable disease, some patients who
correct for sources of bias that cannot be measured, and ulti- ultimately had incurable disease might have been missed (eg,
mately we cannot determine causality (ie, that a PC consulta- patients who received pancreatic surgery and recurred early).
tion itself is causing the decrease in aggressive care near death). However, the magnitude of the bias is likely small. Lastly, although
It is conceivable that the patients and families themselves are we controlled for survival duration in our sensitivity analysis, the
the main determinants of receipt of aggressive care and that persistent survival difference seen in those who received pallia-
PC is simply a “marker” of their shift in thinking from focusing tive care and those who did not, may indicate residual confound-
on cure to maximizing quality of life. However, even in these ing that was not corrected even with the sensitivity analysis.
instances, patients benefit from physician (oncologist or pal- Despite these limitations, our study adds important knowl-
liative care) guidance in order to make informed decisions and edge to what is currently known about the effects of PC,
make appropriate plans. Additionally, our effectiveness findings using a population-based design of more than 5000 patients,
are similar to that of the pivotal efficacy trial by Temel et al. (31). a cancer other than lung cancer, and multiple measures of
7 of 8 | JNCI J Natl Cancer Inst, 2015, Vol.107, No.3
aggressiveness. The results suggest that at a population level, 8. Earle CC, Neville BA, Landrum MB, et al. Evaluating claims-
PC is associated with decreased aggressive care near death. based indicators of the intensity of end-of-life cancer care.
Our work provides an effectiveness analysis of PC in routine Int J Qual Health Care. 2005;17(6):505–509.
clinical practice that clinical trials cannot provide, thereby 9. Keating NL, Landrum MB, Lamont EB, et al. End-of-life care
extending the important work of two recent clinical trials for older cancer patients in the Veterans Health Administra-
(31,45). Given the evidence that aggressive care has been asso- tion versus the private sector. Cancer. 2010;116(15):3732–3739.
ciated with worse quality of life for patients and their families, 10. Earle CC, Landrum MB, Souza JM, et al. Aggressiveness of
is often incongruent with patient wishes (52), and is increas- cancer care near the end of life: is it a quality-of-care issue? J
Clin Oncol. 2008;26(23):3860–3866.
ing over time (41,51), it is our hope that our study will add an
11. Barbera L, Paszat L, Chartier C. Indicators of poor quality end-
important piece to the growing literature on the benefits of
of-life cancer care in Ontario. J Palliat Care. 2006;22(1):12–17.
PC and provide an impetus to increase the availability of PC
12. Warren JL, Barbera L, Bremner KE, et al. End-of-life care for
worldwide.
lung cancer patients in the United States and Ontario. J Natl
Cancer Inst. 2011;103(11):853–862.
Funding 13. Krzyzanowska MK, Barbera L, Elit L, et al. Identifying popula-
tion-level indicators to measure the quality of cancer care for
This work was supported by a 2011 Young Investigator Award women. Int J Qual Health Care. 2011;23(5):554–564.
from the Conquer Cancer Foundation of the American Society 14. WHO Definition of Palliative Care. http://www.who.int/cancer/
of Clinical Oncology, an award from the University of Toronto palliative/definition/en/. Accessed December 16, 2014.
30. Smith TJ, Temin S, Alesi ER, et al. American Society of Clini- 42. Barbera L, Elit L, Krzyzanowska M, et al. End of life care
cal Oncology provisional clinical opinion: the integration for women with gynecologic cancers. Gynecol Oncol.
of palliative care into standard oncology care. J Clin Oncol. 2010;118(2):196–201.
2012;30(8):880–887. 43. Deyo RA, Cherkin DC, Ciol MA. Adapting a clinical comorbid-
31. Temel JS, Greer JA, Muzikansky A, et al. Early palliative care ity index for use with ICD-9-CM administrative databases. J
for patients with metastatic non-small-cell lung cancer. N Clin Epidemiol. 1992;45(6):613–619.
Engl J Med. 2010;363(8):733–742. 44. Gelman A HJ. Data Analysis Using Regression and Multilevel
32. Back AL, Li YF, Sales AE. Impact of palliative care case Regression and Multilevel/Hierarchical Models. New York: Cam-
management on resource use by patients dying of can- bridge University Press; 2007.
cer at a Veterans Affairs medical center. J Palliat Med. 45. Zimmermann C, Swami N, Krzyzanowska M, et al. Early
2005;8(1):26–35. palliative care for patients with advanced cancer: a cluster-
33. Seow H, Piet L, Kenworthy CM, et al. Evaluating a palliative randomised controlled trial. Lancet. 2014;383(9930):1721–
care case management program for cancer patients: the 1730.
Omega Life Program. J Palliat Med. 2008;11(10):1314–1318. 46. Mack JW, Cronin A, Keating NL, et al. Associations between
34. Penrod JD, Deb P, Luhrs C, et al. Cost and utilization outcomes end-of-life discussion characteristics and care received
of patients receiving hospital-based palliative care consulta- near death: a prospective cohort study. J Clin Oncol.
tion. J Palliat Med. 2006;9(4):855–860. 2012;30(35):4387–4395.
35. Tse DM, Chan KS, Lam WM, et al. The impact of palliative 47. Yoong J, Park ER, Greer JA, et al. Early palliative care in
care on cancer deaths in Hong Kong: a retrospective study of advanced lung cancer: a qualitative study. JAMA Intern Med.
article