Integration of Oncology and Palliative Care A Lancet Oncology

Lancet Oncology Commission
Integration of oncology and palliative care: a Lancet Oncology

Commission
Stein Kaasa*, Jon H Loge*, Matti Aapro, Tit Albreht, Rebecca Anderson, Eduardo Bruera, Cinzia Brunelli, Augusto Caraceni, Andrés Cervantes,
David C Currow, Luc Deliens, Marie Fallon, Xavier Gómez-Batiste, Kjersti S Grotmol, Breffni Hannon, Dagny F Haugen, Irene J Higginson,
Marianne J Hjermstad, David Hui, Karin Jordan, Geana P Kurita, Philip J Larkin, Guido Miccinesi, Friedemann Nauck, Rade Pribakovic, Gary Rodin,
Per Sjøgren, Patrick Stone, Camilla Zimmermann, Tonje Lundeby
Full integration of oncology and palliative care relies on the specific knowledge and skills of two modes of care: the Lancet Oncol 2018;
tumour-directed approach, the main focus of which is on treating the disease; and the host-directed approach, which 19: e588–653
focuses on the patient with the disease. This Commission addresses how to combine these two paradigms to achieve Published Online
October 18, 2018
the best outcome of patient care. Randomised clinical trials on integration of oncology and palliative care point to
http://dx.doi.org/10.1016/
health gains: improved survival and symptom control, less anxiety and depression, reduced use of futile chemotherapy S1470-2045(18)30415-7
at the end of life, improved family satisfaction and quality of life, and improved use of health-care resources. See Comment page e565, e568,
Early delivery of patient-directed care by specialist palliative care teams alongside tumour-directed treatment promotes e570, and e572
patient-centred care. Systematic assessment and use of patient-reported outcomes and active patient involvement in *Contributed equally
the decisions about cancer care result in better symptom control, improved physical and mental health, and better use European Palliative Care
of health-care resources. The absence of international agreements on the content and standards of the organisation, Research Centre, Department
education, and research of palliative care in oncology are major barriers to successful integration. Other barriers of Oncology, Oslo University
Hospital and Institute of
include the common misconception that palliative care is end-of-life care only, stigmatisation of death and dying, and Clinical Medicine, University of
insufficient infrastructure and funding. The absence of established priorities might also hinder integration more Oslo, Oslo, Norway
widely. This Commission proposes the use of standardised care pathways and multidisciplinary teams to promote (Prof S Kaasa PhD,
integration of oncology and palliative care, and calls for changes at the system level to coordinate the activities of Prof J H Loge PhD,
T Lundeby PhD,
professionals, and for the development and implementation of new and improved education programmes, with the M J Hjermstad PhD); Institute of
overall goal of improving patient care. Integration raises new research questions, all of which contribute to improved Basic Medical Sciences, Faculty
clinical care. When and how should palliative care be delivered? What is the optimal model for integrated care? of Medicine, University of Oslo,
What is the biological and clinical effect of living with advanced cancer for years after diagnosis? Successful integration Oslo, Norway (Prof J H Loge);
Genolier Cancer Centre,
must challenge the dualistic perspective of either the tumour or the host, and instead focus on a merged approach Clinique de Genolier, Genolier,
that places the patient’s perspective at the centre. To succeed, integration must be anchored by management and Switzerland (M Aapro MD);
policy makers at all levels of health care, followed by adequate resource allocation, a willingness to prioritise goals and Centre for Health Care
(T Albreht PhD), and Centre for
needs, and sustained enthusiasm to help generate support for better integration. This integrated model must be
Promotion and Prevention
reflected in international and national cancer plans, and be followed by developments of new care models, education Programme Management
and research programmes, all of which should be adapted to the specific cultural contexts within which they are (R Pribakovic MD), National
situated. Patient-centred care should be an integrated part of oncology care independent of patient prognosis and Institute of Public Health,
Ljubljana, Slovenia; Marie Curie
treatment intention. To achieve this goal it must be based on changes in professional cultures and priorities in
Palliative Care Research
health care. Department, Division of
Psychiatry, University College
Introduction families. Now, for the most part, oncological and London, London, UK
(R Anderson MSc,
The overall aim of this Commission is to show why and palliative care cultures are still separate.
Prof P Stone MD); Department
how palliative care can be integrated with oncology for Research on integrating oncology and palliative care is of Palliative, Rehabilitation
adults with cancer, irrespective of treatment intention, heterogeneous. Almost all studies have been done and Integrative Medicine,
in high-income and middle-income countries. This in high-income countries, but the variation across University of Texas MD
Anderson Cancer Center,
integration will combine two main paradigms, tumour countries, systems, and settings often limits the gener
Houston, TX, USA
directed and patient (host) directed, through the use of alisability of findings. The 2018 Lancet Commission (Prof E Bruera MD, D Hui MD);
the most effective and optimal resources from oncology report on palliative care focusing on low-income and Palliative Care, Pain Therapy
and palliative care in well-planned, patient-centred care middle-income countries stated, “Poor people in all and Rehabilitation Unit,
Fondazione IRCCS Istituto
pathways. parts of the world live and die with little or no palliative Nazionale dei Tumori di Milan,
The two paradigms might be understood to be care or pain relief.”1 That Commission gave a series of Milan, Italy (C Brunelli PhD,
representing two different cultures. Oncology has roots recommendations, such as how to quantify serious Prof A Caraceni MD);
in mainstream medicine (ie, internal medicine), and is health-related suffering, and proposes an Essential Department of Medical
Oncology, Biomedical Research
primarily based on the acute care model. From the mid Package of palliative care, which might also be relevant Institute INCLIVA, CiberOnc,
1960s, hospice and palliative care were established to high-income countries as a basic benchmark of University of Valencia,
outside the main health-care systems, often financed by successful implementation at the patient level. Their Valencia, Spain
charities. At the time, the primary focus of palliative previous Commission also recommended international (Prof A Cervantes PhD);
IMPACCT, Faculty of Health,
care was end-of-life care, with care provided by and collective action to receive universal coverage of University of Technology
multidisciplinary teams working with patients and their palliative care and pain relief, and better evidence and
www.thelancet.com/oncology Vol 19 November 2018 e588

The Lancet Oncology Commission
Sydney, Sydney, NSW, Australia priority-setting tools to measure the global need for one or the other,7 and neither ESMO nor ASCO
(Prof D C Currow PhD); Wolfson palliative care and implementation policies. Given the differentiate between the content of supportive care and
Palliative Care Research Centre,
Hull York Medical School,
empirical basis presented in the 2018 Lancet palliative care. Despite a similar focus, the starting points
University of Hull, Hull, UK Commission, the recommendations are primarily for palliative and supportive care differ; whereas palliative
(Prof D C Currow); End-of-Life focused on high-income countries, but the findings, care started as end-of-life care, supportive care initially
Care Research Group, Vrije experiences, and models presented might be highly focused side-effects of anticancer treatment, such as
Universiteit Brussel and Ghent
University, Brussels, Belgium
relevant to other contexts as well. chemotherapy-induced nausea and vomiting, and
(Prof L Deliens PhD); The WHO definition of palliative care states that the neutropenia. The overall goal of palliative care is to
Department of Medical competence, attitudes, and skills of palliative care should improve the patient’s quality of life congruent with the
Oncology, Ghent University be integrated in health care in general and in cancer care, patient’s preferences—ie, the patient (host)-centred
Hospital, Ghent, Belgium
(Prof L Deliens); Institute of
“Palliative care is an approach that improves the quality perspective. Thus, improve ment of function, optimal
Genetics and Molecular of life of patients and their families facing the problem symptom management, mobilisation of resources and
Medicine, University of associated with life-threatening illness, and is applicable active involvement of patient and family throughout the
Edinburgh, Edinburgh, UK early in the course of the illness, in conjunction with care process are key components. This improvement can
(Prof M Fallon MD); WHO
Collaborating Center for
other therapies that are intended to prolong life.”2 The be achieved by an integration of oncology and palliative
Palliative Care Public Health present paper accepts, but builds on this definition, care guided by the patient’s needs
Programs, Catalan Institute of which differs substantially from the common perception Symptom management is a key element of both
Oncology, University of
of palliative care as being synonymous with end-of-life supportive and palliative care. Symptoms inform
Vic/Central Catalonia,
Barcelona, Spain care. diagnosis and treatment in all parts of medicine, and
(Prof X Gómez-Batiste PhD); Hospital-based specialised palliative care alongside play a central role throughout the disease trajectory. They
Regional Advisory Unit for tumour-directed and life-prolonging treatment has been are a particular focus in palliative care, in that symptom
Palliative Care, Department of
shown to contribute to better oncology care for patients alleviation is the main target for interventions.2 Symptom
Oncology, Oslo University
Hospital, Oslo, Norway and families, in terms of better symptom management, assessment is often not done systematically in oncology
(K S Grotmol PhD); Department quality of life, satisfaction with care, and less psycho practice or not routinely incorporated into the clinical
of Supportive Care, Princess logical distress; some studies even suggest survival decision-making processes.
Margaret Cancer Centre,
benefits.3–5 Thus, we think it is timely to rethink and WHO defines integrated health services as “the
University Health Network,
Toronto, ON, Canada reorganise the delivery of oncology and palliative care to organization and management of health services, so that
(B Hannon MD, Prof G Rodin MD, improve treatment and promote collaboration at the people get the care they need, when they need it, in ways
Prof C Zimmermann PhD); appropriate levels of care. We propose models of that are user-friendly, achieve the desired results and
Division of Medical Oncology,
integration that fit the tasks and responsibilities of the promote value for money”.8 In oncology, the multi
Department of Medicine
(B Hannon, two main hospital categories—ie, university hospitals disciplinary team approach that combines competence
Prof C Zimmermann), Institute (tertiary) and local hospitals (secondary), and community and skills in the planning of treatment care has become
of Medical Science health care (primary). standard.9 This approach is an integration of disciplines
(Prof G Rodin), and Department
of Psychiatry (Prof G Rodin,
Integration of care is a complex intervention based on at the hospital level of care (eg, among surgeons,
Prof C Zimmermann) University organisational structure and patient-centred plans. The oncologists, pathologists, radiologists, and specialist
of Toronto, Toronto, ON, use of standardised care pathways (SCPs) is a method or nurses). The multidisciplinary team can include palliative
Canada; Regional Centre of planning tool for the implementation of such complex care specialists at any stage of the disease trajectory,
Excellence for Palliative Care,
Western Norway, Haukeland
processes. The European Pathway Association (EPA) irrespective of whether treatment intention is curative,
University Hospital, Bergen, defines SCPs as “a complex intervention of the mutual life-prolonging, or palliative. Given the definition of
Norway (Prof D F Haugen PhD); decision making and organisation of care processes for a palliative care, interventions provided by palliative care
Cicely Saunders Institute of well-defined group of patients during a well-defined have a broad focus and can therefore not be delivered by
Palliative Care, Policy and
Rehabilitation, King’s College
period”. SCPs facilitate transitions within hospitals and a single profession; multiple professions organised in
London, London, UK between health-care levels, which should be seamless, to teams are therefore common. The composition of the
(Prof I J Higginson PhD); ensure the continuity and coordination of care. The teams might vary, depending on local resources and
Department of Medicine, present Commission proposes the use of SCPs as a traditions, and the internal organisation of the teams
Haematology, Oncology and
Rheumatology, Heidelberg
method for the integration of oncology and palliative care. might also vary, but multidisciplinarity, which draws on
University Hospital, Supportive care and palliative care focus on the knowledge from different disciplines but stays within
Heidelberg, Germany patient—the host of the cancer—whereas the primary their boundaries,10 are probably the most common
(Prof K Jordan MD); Palliative focus in oncology is on the tumour. During the past internal organisation. The term multidisciplinary teams
Research Group, Department of
Oncology (G P Kurita PhD,
15 years, semantic discussions have been had regarding will therefore be used throughout this Commission.
Prof P Sjøgren PhD) and definitions and distinctions between supportive and From a societal, ethical, and political perspective, the
Multidisciplinary Pain Centre, palliative care. The European Society for Medical escalating costs of health care are a major problem.
Department of
Oncology (ESMO) states that supportive care should be Although spending on cancer care comprises only 5% of
Neuroanaesthesiology
(G P Kurita), available at any stage of the disease, whereas palliative the overall health-care budget,11 these costs continue to
Rigshospitalet–Copenhagen care is focused on treatment when cure is no longer rise more rapidly than in other health-care areas.12 The
University Hospital, Denmark; possible.6 The American Society of Clinical Oncology escalating costs can be attributed to the ageing of the
Department of Clinical
(ASCO) does not specify a particular time for delivery of population, new and expensive diagnostic and treatment
e589 www.thelancet.com/oncology Vol 19 November 2018

options, more prolonged survival of patients with mation sharing, including discussion of prognosis and Medicine, Faculty of Health
metastatic disease, and a growing public demand for options for supportive care, are often missing from and Medical Sciences,
University of Copenhagen,
tumour-directed treatment at all stages of the disease. interviews.28 A more patient-centred focus might be Copenhagen, Denmark
The increased complexity and escalating costs also apply enhanced by a multidisciplinary team approach, with (Prof P Sjøgren); Centre
to care at the end of life; about a third of the cost of cancer systematic collaboration among team members from Hospitalier Universitaire
care is spent during the patient’s last year of life.13 different professions within and across levels of care. Vaudoise and Institut
Universitaire de Formation et
Planning and structure of cancer care and palliative care This implies an empathic approach by health-care de Recherche en Soins,
has the potential to reduce costs, especially when the professionals with willingness and skills to assess and University of Lausanne,
complexity of treatment and care increases.14 understand the patient’s needs. Health-care providers Switzerland
Evidence-based medicine is the norm in oncology need to understand, accept, communicate, and plan for (Prof P J Larkin PhD); Clinical
Epidemiology Unit,
practice, but evidence as to when to start and stop home care because most patients want to spend as much Oncological Network,
anticancer treatment near the end of life has been time as possible at home during their last phase of life. Prevention and Research
scarce.15 The quality and quantity of research in this area Institute, Florence, Italy
has been questioned.16,17 This also applies to research on Palliative care and oncology care—development (G Miccinesi MD); Department
of Palliative Medicine,
the effects of newly registered targeted therapies and over the past four decades University Medical Center
immunotherapies. There is little scientific evidence for In this section we briefly outline the developmental and Göttingen,
the effect of chemotherapy in most areas of symptom conceptual issues of relevance to the present focus on Georg-August-Universität
Göttingen, Göttingen,
management, including the treatment of pain,18 although integration of oncology and palliative care. For years
Germany (Prof F Nauck PhD)
palliative radiotherapy might be highly effective in that cancer care has been criticised for its disproportionate
Correspondence to:
regard.19 focus on the tumour, compared with attention to the Prof Stein Kaasa, European
It is especially important during the patient’s last year of patient with the cancer. The concept of hospice care, and Palliative Care Research Centre,
life that the attention given to the effect of tumour-directed later palliative care, was introduced partly as a reaction to Department of Oncology, Oslo
treatment is congruent with the individual patient’s the absence of a patient-centred focus. Attention to University Hospital and Institute
of Clinical Medicine, University of
perception of benefits, in terms of symptom burden and palliative cancer care emerged in the 1970s, partly Oslo, Oslo 0424, Norway
quality of life.20 Few, if any, trials give guidance for such through efforts of researchers such as Jan Stjernswärd, [email protected]
choices. This has led to the recommendation that a set of who was attached to WHO at that time.29 The term For the European Pathway
criteria (eg, disease progression, performance status, palliative care was probably first coined by the Canadian Association see http://e-p-a.org/
nutritional status, weight loss, and symptom burden) surgeon Balfour Mount in 1974.30 At the time, palliative
should guide the discontinuation of tumour-directed care had a strong focus on end-of life-care and it is
treatment.21,22 These criteria could also apply to phase 1 commonly still equated with this timeframe,31 despite its
trials, which might have therapeutic intent, but for which subsequent redefinition. A dichotomised perception of
the likelihood of benefit to the individual patient might be oncology care and palliative care is outlined in figure 1.
extremely small.23 As the disease progresses, the main This perception fits with palliative care as equal to end-of-
outcomes of treatment should be continually assessed and life care, but is not in line with the present definition of
redefined as they vary from tumour response to symptom palliative care as formulated by WHO (“applicable earlier
control, preservation of function, and wellbeing.24 in the disease trajectory”).2 A perception in line with this
Shared decision-making (SDM) is a key element of definition, in which the two are integrated or given in
cancer care, but the degree to which patients can parallel, is outlined in figure 1.
participate as active partners in the decision-making
process has been questioned, when multiple options for
Traditional palliative care
tumour-directed treatment are available and when life-
prolonging treatment with marginal benefits are offered.25
Some patients want to live as long as possible and are Palliative care to
manage symptoms
willing to try intensive treatment, even if the likelihood of Life-prolonging or curative treatment and improve quality
benefit is extremely small and the risk of side-effects that of life
might impair quality of life and reduce residual time at
home is high.26 Active patient participation presupposes Diagnosis Death
sufficient and relevant knowledge of the disease and
treatment options. This amount of knowledge can only be Early palliative care
reached by the continuous provision of realistic patient-

centred information. To provide this information, good Life-prolonging or curative treatment
communication skills among the oncologists and

palliative care specialists are required, and the needs and
Palliative care to manage symptoms and improve quality of life
wishes of patients and families need to be assessed
systematically and used in the decision-making Diagnosis Death
processes.27 For decision making for phase 1 trials,
fundamental components of communication and infor Figure 1: Traditional versus early palliative care

Supportive care emerged as a concept and care approach The content and professional competence needed to
in the late 1980s, somewhat later than palliative care, but provide palliative care and supportive care are similar,
with a similar focus on the individual patient with cancer, with both focusing on the host—the patient living with
the host, not the tumour.32 Supportive care focused on the the disease or with side-effects after the treatment, or
entire disease trajectory, including when curative both. Palliative care and supportive care are differently
treatments, often accompanied by multiple side-effects, are organised across locations, on the basis of resources and
still being delivered. Late effects began to receive attention traditions. In some centres, the two are organised as one
during the 1980s as new health problems in cancer care, service, whereas in others they are completely separate.
and spawned the field of cancer survivorship, which can be Independent of organisational structure, the focus on the
regarded as an extension of supportive cancer care.33,34 host with a patient-centred focus is similar. Therefore,
The difference between palliative care and supportive when resources permit, integration of palliative care and
care is primarily related to differences in the stage of supportive care might be most effective in terms of
disease to which they are applied, rather than to the treatment delivery and as a direction to strengthen the
treatment itself.35 This is reflected in the similar patient-centred culture in cancer care delivery.
definitions of the concepts by the US National Cancer WHO’s most recent (2002) definition of palliative care,
Institute (NCI) and WHO.36 According to the WHO revised from its 1989 definition, points to the integration
definition, palliative care focuses on patients with a life- of oncology and palliative care by stating, “Palliative care
limiting disease, whereas supportive care is applicable is applicable early in the course of illness, in conjunction
irrespective of treatment intention and might also include with other therapies that are intended to prolong life,
rehabilitation of cured cancer survivors. Therefore, in such as chemotherapy or radiation therapy, and includes
our view, treatments of pain, fatigue, physical, and those investigations needed to better understand and
psychological distress after curative treatment are best manage distressing clinical complications.”37 The inte
characterised as supportive care. grated care model has also become a topic in cardiology,
pulmonology, and other specialties.
Health-care system
Patients live longer with metastatic disease—the need
for coordination and planning
The possibilities for tumour-directed treatments have
General Local Cancer
practitioner hospital centre increased exponentially during the past decade. Multiple
treatment lines have become the rule for common
cancers, such as breast, lung, colorectal, and prostate
Standardised care pathways
cancer, and many more patients are now living with
metastatic disease. New immune therapies are being
introduced to standard oncology care, with side-effects
that differ from those of traditional chemotherapeutic
Cancer centre
agents. We do not have systematic data on the effect of
these new therapies on the host and their clinical
presentations; however, we do know that the increase in
the number of patients living with advanced disease will
Colonoscopy Imaging Pathology Surgery have implications on coordination and planning of care,
laboratory MRI
and will require the combination of tumour-centred and
the patient-centred approaches.
Standardised care pathways This development has reshaped cancer into a chronic
illness, with WHO recognising cancer as one of four
major chronic diseases in 2010.38 The development has
Department of oncology also made the terms curative and palliative tumour-
directed treatment even more vague and prone to
misunderstanding by patients and possibly some medical
staff. We prefer terms related to treatment intention; ie,
curative, life prolonging, or palliative.39 An increasing
Medical Radiation Cancer
oncology oncology palliative care number of patients with advanced cancer will probably
die from other comorbid diseases after a prolonged
Standardised care pathways period of tumour-directed treatment; thus, the chronic
care model will become increasingly relevant for
oncology–palliative care. However, the traditional disease
model still dominates within cancer care. The chronic
Figure 2: Health care includes silos at different levels care model was launched at the end of the 20th century,

and represents a paradigm shift within health care.40 The

model emphasises patient-centred elements (eg, patient Panel 1: Three levels of integration
empowerment, patient preferences, and family and Linkage
social support)40 and therefore has obvious similarities • Patients are cared for in a planned system
with patient-centredness, although the two seem to have • Based on an understanding of special needs (formalised in
been developed in parallel. a standardised care pathway)
• Work in parallel or in series
Integration in health care • Basic understanding of the various professional skills
The availability of new tumour-directed treatments for
advanced cancer points to a basic challenge in health care Coordination
in general and in cancer care specifically: how can • Patients are cared for in a well-structured plan, on the
complex care pathways be organised in a flexible and basis of patients’ needs and the content of the
optimal structure, involving multiple professionals standardised care pathway
working simultaneously or in parallel? Health care is • Integration operates in separate structures within a
currently most often organised in silos of primary, system (eg, pathology, imaging, surgery, radiation, or
secondary, and tertiary levels of care, with levels within tumour-directed chemotherapy symptom management)
each silo as well. Surgical oncology, medical oncology, • Integration has been an implementation plan
radiation oncology, and palliative care within the cancer (of the standardised care pathway) and follow-ups and
centre are examples of such silos, organised with separate monitoring of the plan
leaders from different departments with individual Full integration
budgets. Patients and their families might experience • Resources (competence and skills of medical staff) are
great difficulty navigating between and within each of pooled into one unit or section, taking from existing
these silos, and understanding mixed messages about systems
the main focus of care presented by two different cultures • Silos are eliminated (partially or totally) and the
within the same department or hospital. As exemplified organisation is based on the standardised care pathway
in figure 2, these silos should be connected to provide the • The multidisciplinary team meetings can, as a dynamic
varying needs for care of each individual patient. SCPs structure, be an example of full integration as they meet
can be used to foresee, establish, and administer such
Panel adapted from Leutz.42
connections.
In 2007, the WHO Director-General Margaret Chan
stated, “We need a comprehensive, integrated approach
to service delivery. We need to fight fragmentation.”41 The In an influential article, Leutz42 defined integration as
current challenge to service delivery is the specification “the search to connect the health care system with other
of the nature of integrated services in different settings, human service system to improve outcome (clinical,
and the establishment of how integration can contribute satisfaction and efficiency)”. He proposed three levels of
to the intended aim of ensuring that patients with cancer, integration: linkage, coordination, and full integration.
and their families, receive the care they need. The WHO In panel 1, examples and understanding of these three
technical brief8 on the inte gration of health services levels are provided from a general health-care perspective
aimed to show that integrated service delivery is best and from an oncology or palliative care perspective, or
seen as a continuum involving technical discussions both. The levels of integration can be understood as both
about tasks that need to be done to provide good-quality static and dynamic. Integration as outlined in this panel
health. challenge the internal life and individual priorities in
Integration aims to coordinate the activities of cultures and subcultures in both oncology and palliative
professionals, with the overall goal of improving patient care. To reach achievable and practical solutions,
care. The achievement of such coordination requires integration can be formalised and made routine in some
change at the system level on the basis of a common situations (eg, multidisciplinary team meetings as one
understanding and acceptance of the two paradigms in component in a planned structure [SCPs]), or added
this context. From an organisational perspective, the flow according to patient needs to optimise care in other
of patients between levels, or silos, of the organisation situations.
(ie, units, sections, departments, or hospitals) needs to be
taken into account. To reach the goal of integration, a Integration of oncology and palliative care
common understanding of a merging of the two paradigms, The term integration has been applied to the interplay
as well as budgetary reallocations and formal or informal between oncology and palliative care for decades; it
changes in the organisation, are probably needed. These was used by Malin in 2004,43 in an editorial that
changes might allow more flexible allocation of human recommended efforts be made to bridge the gap between
and treatment resources according to the needs defined in oncology and palliative care to provide better care
the SCPs. for those dying from cancer. The distinction between

Jordhøy et al Temel et al Zimmermann Bakitas et al Maltoni et al Temel et al Grønvold et al

(2000)47 (2010)3 et al (2014)5 (2015)48 (2016)49 (2017)50 (2017)51
Clinical structure
Palliative care inpatient consultation team Y Y Y Y ·· Y Y
Palliative care outpatient clinic Y Y Y Y Y Y Y
Community-based care or home palliative care Y ·· Y ·· ·· ·· ··
Clinical processes
Multidisciplinary specialised palliative care team Y Y Y Y Y Y Y
Routine symptom screening in the outpatient ·· ·· ·· ·· ·· ·· ··
oncology clinic
Administration of systemic cancer therapy Y Y Y Y Y Y Y
(eg, chemotherapy and targeted agents) possible
in patients admitted to palliative care service
Follow prespecified palliative care guidelines Y Y ·· ·· Y Y Y
Early referral to palliative care Y Y Y Y Y Y Y
Availability of clinical care pathways (automatic ·· ·· ·· ·· ·· ·· ··
triggers) for palliative care referral
Palliative care team routinely involved in ·· Y ·· ·· ·· ·· ··
multidisciplinary tumour conference for patient
case discussions
Communication, cooperation, and coordination Y Y ·· ·· Y ·· ··
between palliative and oncology service
Routine discussion of prognosis, advance care Y Y Y Y Y Y Y
planning with goals of care
Y=presence of component in trial. Table adapted from Hui and colleagues.44,52
Table 1: Components of integration from seven randomised trials
integration and early integration has not been clearly published reviews of the effectiveness of specialised
defined, but use of early integration might help to palliative care have mainly been based on mixed
counteract the commonly held belief that palliative care populations, without separation of the results for patients
is equivalent to end-of-life care. The strong focus on with cancer. The trials included in the 2017 review were
integration in contemporary oncology and palliative care published between 2001, and 2016, and all used different
has also led to experts formulating consensus-based designs and endpoints. The components of integration
indicators of integration.44 from the seven randomised trials included in the 2017
Temel and colleagues’ findings3 of improved survival review are shown in table 1.44,52
and better quality of life with early palliative care has At the turn of this century, Jordhøy and colleagues47
paved the way for the integration of palliative care in published the results of a cluster-randomised trial of
oncology as a means to provide better and more palliative care. We are not aware of any randomised trials
patient-centred care for patients with a life-limiting on the effects of palliative care programmes before this
cancer. Palliative care has also been proposed as a means publication. Some trials in the 1980s and early 1990s tried
to offset the rapidly increasing costs in oncology, to evaluate the effects of elements included in palliative
especially in the patients’ last year of life, and to address care, such as end-of-life care, with negative results.53–55
the anticipated shortage of resources due to increasing These early trials were hampered by methodological
demands and costs. Temel and colleagues’ study3 led to shortcomings, such as an absence of well-defined primary
the formulation of an ASCO provisional clinical opinion endpoints, control contamination, and problems with the
in 2012,45 which was revised into a clinical practice recruitment processes, and problematic attrition and
guideline in 2017.15 Without using the term early adherence. In their large study47 of mixed cancer diagnoses
integration, the provisional clinical opinion stated using well-validated instruments, Jordhøy and colleagues
palliative care is more than end-of-life care, and that circumvented many of these limitations; however, the main
patients would benefit from receiving palliative care focus of this comprehensive trial was integration of
while still receiving tumour-directed treatment, based on community and hospital care for patients with advanced
a low to medium amount of evidence.45 cancer. More patients died at home in the intervention
The current research on integration of oncology and group, compared with the control group, and these patients
palliative care primarily stems from studies of patients also spent less time in hospitals and more time at home
with cancer in outpatient hospital settings, and this and in nursing homes. No effect on symptom burden was
research has been synthesised in a 2017 review.46 Other shown, which was reported in a separate article.4

Several years later, Bakitas and colleagues56 designed first European trial to confirm the results of the important
ENABLE II, a randomised trial to test a telephone-based North American trials.3,5
psychoeducational palliative care intervention delivered Temel and colleagues’ 2017 study50 again drew attention
concurrent with oncological treatment. The programme to early palliative care by examining the effect of an
was found to significantly improve both mood and quality integrated palliative care model on patients with newly
of life in a sample of 322 patients with mixed cancer diagnosed gastrointestinal (non-colorectal) cancer and
diagnoses. However, a traditional palliative care model patients with lung cancer. In addition to improved quality
was not applied, because the study did not systematically of life and decreased depression, they showed that an
include the intervention of a (multidisciplinary) palliative integrated palliative care model improved the patients’
care team. ability to cope with their prognosis and enhanced their
Temel and colleagues’ study3 is usually referred to as the communication with clinicians about end-of-life
landmark trial of integration of oncology and palliative preferences. They showed that these positive effects vary
care. They showed, among patients with newly diagnosed by cancer types, but the two subsamples were too small
lung cancer, early palliative care not only reduced to substantiate these differences.
depression and symptom burden, and improved quality of The 2017 Danish palliative care trial (DanPaCT)51
life, but also produced a survival benefit. The intervention investigated the effect of a palliative care intervention
group reported improved prognostic awareness and among patients with a range of cancer diagnoses. Patients
received less intensive cancer treatment at the end of life. were included if they scored above a predefined threshold
However, the study was carried out in a highly specialised for self-reported symptoms or reduced functioning.
institution and some researchers have raised doubt as to The primary outcome was defined as the individual
its generalisability to other care settings.57 patient’s main problem, as defined by a screening
In a cluster-randomised trial in 2014, Zimmermann process. The sample was large with little loss to follow-up.
and colleagues5 investigated early involvement of No differences in either primary or secondary outcomes
specialised palliative care in the treatment of patients were reported. Grønvold and colleagues51 proposed
with a wide range of advanced cancers. This study several possible explanations for the absence of beneficial
provided evidence of benefits on quality of life and effects, including the absence of structure in the palliative
symptom burden, and was the first study to explore care visits and short observation time.
clinician-patient interactions, by specifically addressing A 2018 study58 confirmed Temel and colleagues’ 2010
the relationship with health-care providers and patients’ findings;3 however, the intervention was not palliative care
problems in their interactions with nurses and doctors per se, but consisted of monthly sessions with a palliative
(related to information seeking and communication). care nurse and inferred more use of consultations with a
The intervention group was more satisfied with care than psychologist. The study therefore adds to the variability in
the control group, but no differences were found in other the content of the palliative services (ie, the intervention)
measures of patient-staff interactions. and of how palliative care and oncology care are delivered
In the meantime, the initial model constituting in studies of integration of oncology and palliative care,59
ENABLE II had been expanded, and, in 2015, Bakitas and but the added element was patient centred, which is of
colleagues48 published the findings of the ENABLE III particular relevance in this context.
trial. Through the application of a fast-track design, this The growing body of evidence for integration of
trial was the first to evaluate the optimal timing for the oncology and palliative care has been synthesised in
concurrent introduction of palliative care and standard reviews, statements, and guidelines, some of which focus
oncological care.48 The only difference between the specifically on integration and others more generically on
groups was longer 1-year survival for the group who specialised palliative care.15,57,60–62 Several issues complicate
received care early compared with the group who started attempts to evaluate and compile this literature. Most of
palliative care 3 months later. The intervention consisted the reviews underline that the heterogeneity in settings,
of an initial in-person palliative care consultation by a target populations, and study outcomes make it difficult
certified palliative care physician, followed by six to directly compare trials. The diversity in intervention
structured phone coaching sessions by an advanced content and the palliative care-specific component are
practice nurse using standardised curriculum. This type particularly cumbersome (table 1). In addition, the
of intervention raises the question of whether ENABLE III variability in methodological quality across trials was
is a sophisticated psychoeducational model, rather than a highlighted in a 2016 meta-analysis.63 When only trials
specialised palliative care intervention. with low risk of bias were considered, the authors
In 2016, in a multicentre randomised trial, Maltoni and concluded that the evidence for the effectiveness of
colleagues49 evaluated early palliative care efficacy for specialised palliative care interventions for improving
patients with advanced pancreatic cancer through both quality of life and symptom burden is relatively weak.63
patient-reported outcomes and health-care use. They However, a 2017 Cochrane review64 concluded that early
reported benefits in quality of life, symptom burden, and palliative care might have more beneficial effects on
reduced time spent in institutions. As such, this was the quality of life and intensity of symptoms among patients

with advanced cancer than among those given usual or life-prolonging, tumour-directed treatment ceases. The
standard cancer care alone. The effects are of clinical infrequent assessment of symptoms is a major factor
relevance for patients at an advanced disease stage with explaining inadequate symptom relief, with undue
limited prognosis, when further decline in quality of life suffering among patients with cancer who are
is the rule. approaching end of life. A key symptom in health care is
The heterogeneity in study outcomes and metho pain, and, according to the international definition by the
dological quality of studies of the effectiveness of palliative International Association for the Study of Pain,70 pain can
care are obvious limitations in research on integration. only be assessed reliably and validly by self-report, not by
However, although the evidence for integration of observations. Several other symptoms, only assessable by
oncology and palliative care might seem meagre, the patient report (ie, as PROMs), are important to consider
recommendation to integrate is strong because the overall in the care of patients with cancer. These include
picture shows that different kinds of early palliative care psychological symptoms (eg, anxiety and depression)
interventions have a positive effect on various patient and somatic symptoms (eg, anorexia, dyspnoea, fatigue),
outcomes. and overall quality of life.
Traditionally, PROMs were collected through the use of
Systematic symptom assessment paper-based questionnaires. Advances in health infor
To facilitate better patient involvement in cancer care and mation technology have prompted the development of
improved patient-centred outcomes, the patient’s voice electronic tools for the distribution of PROMs. Such tools
must be heard by their medical team during shared allow an effective integration of patient-related data from
decision-making, in terms of symptoms, functions, various sources, and permit follow-up from a distance of
quality of life, and preferences for information provision. patients who are not admitted to hospital or seen in
The recognition of the patients’ perspectives by health- consultations, and can promote data sharing between
care providers as valuable or even decisive when choosing care teams at different care levels. In oncology, electronic
how to care, where to care, and when to care, represents a assessments and rapid presentation of results facilitate
major shift in medicine over the past 10–20 years. communication, are perceived positively by patients and
Patients’ perspectives have now been recognised as valid clinicians, and might result in a more efficient and
outcomes in clinical medicine, as endorsed by the focused use of time.71,72 Further, a 2012 qualitative study73
National Institute of Health consensus conference.65 showed perceived usefulness of an electronic tool might
Although systematic symptom assessment is an be more important than functional aspects such as user-
established core clinical activity in palliative care, directly friendliness and speed to encourage its use. Immediate
derived from the WHO definition, symptom assessment display of easily interpretable results to the health-care
is still rarely done systematic or actively used in the providers is a crucial factor for successful implementation
patient decision-making processes in oncological and of electronic registration of PROMs into the clinics.74
palliative care practices. On the basis of this background information, we find it
In 2006, the US Food and Drug Administration (FDA) pertinent to point to a 2016 study75 on the effects of
proposed the term patient-reported outcomes measures systematic symptom assessment by tablet computers in
(PROMs) for all measures that can best, or only, be patients with advanced solid tumours. The study showed
assessed by asking the patients themselves.66 By that, the positive outcomes of systematic symptom assessment in
FDA also formally recognised the importance and oncology practice, and that health-related quality of life
clinical utility of PROMs by releasing a new guideline for improved among the intervention group and worsened
industry on these issues. PROMs are therefore an among those receiving usual care. In a separate letter,76
umbrella term covering the patient’s perspective on the authors showed improved survival among those who
physical and psychological wellbeing, and symptoms and had their symptoms assessed systematically. The results
treatment effects.67 The recognition of PROMs as of this trial are a strong reminder of the importance and
independent outcomes in cancer68,69 is consolidated by positive effects of systematic symptom assessment in
the CONSORT-PRO extension statement69 developed to cancer care in general.
improve the reporting of PROMs on patients’ evaluation
of symptoms, functioning, and quality of life. Because Standardised care pathways
the patient is the primary source of information, PROMs Integrated care models can be understood as organ
supplement clinical observations and objective findings isational methods to solve the challenges of management
with individual patient information. of complex care processes, and particularly so in the
Symptom assessment tools are, for these reasons, growing elderly population. In integrated care, profes
grouped under the umbrella PROMs, which also encom sionals with different competencies and from distinct
passes other outcomes assessed similarly, such as quality organisations work together in complex and formalised
of life and functional status. Symptom assessment is structures. This model challenges the traditional vertical
pivotal for palliative care and supportive care efforts organisation of health care, as outlined earlier, structured
throughout the disease trajectory, and increasingly so as in pillars or silos.

Patients often experience gaps between services when were monitored in the SCP group through the use of
they must shift to a new level of care or specialisation.77 computer technology.82 A main feature of the included
A different matrix is hypothesised to better meet the trials was that the SCP was applied in a facility-specific
patient’s needs, which are complex and shifting over manner for a defined period of time, disregarding other
time, and to allow the patient to move between care levels elements involved in patient care and follow-up. Because
or specialisations in way that is more predictable and the SCPs tested were mainly paper based, the potential
transparent to the patient and to their care providers. For utility of a common and flexible electronic SCP was not
this to occur, communication and collaboration among evaluated. The way in which different SCPs were audited
the health-care providers must also be predictable and was also highly variable.81
clearly understood, with the roles of team members
clarified and agreed on. Conclusions
The achievement of integration among the different There is now a strong consensus for integration of
services and levels of health care is by no means oncology and palliative care in contemporary cancer care.
straightforward, because two different cultures with The newly released ASCO guidelines on the topic were,
different foci—ie, the tumour-centred and patient- for months, the most searched article in the Journal of
centred pathways—need to join forces and attend to the Clinical Oncology.15 The published randomised trials on
patient’s needs during the development and imple the subject point to health gains resulting from
mentation of the SCPs. Indeed, the greater the number integration, but what, when, and how to integrate are yet
of actors involved in a patient’s care, the more difficult to be established. Despite clear recommendations for
the communication and coordination. The development integration, this Commission has not identified any
of SCPs is a method for meeting these challenges. health-care system where the content and the constructs
With roots in the automobile and production of integration are implemented. This Commission will
industries, multiple SCPs have been developed and work on the assumption that broad implementation
published over the past 5 years, covering a wide area of plans are needed, adapted to national, regional, and local
health services, ranging from surgical procedures to organisations of oncology and palliative care, as well as
complex disease trajectories.78 Implementation of SCPs the culture of the organisation. Local variations, in terms
ensures care is organised with the right people, at the of resources and practices, also probably play a role.
right time, in the right place. Therefore, SCPs can work By acknowledging integration of oncology and palliative
as a systematic way to organise integration in the or care as a complex process including different parts of the
ganisation to improve patient care and resource use; health-care system, both horizontally and vertically, and
however, such organisation requires the possibility of involving the patient, we propose SCPs as a means by
seamless patient flow in a customised organisational which future efforts could promote integration. For the
model. same reasons, this Commission will address integration
A wide range of methods have been used in the in different sections. Each section will address different
development of SCPs, mainly without a common aspects of integration, ranging from how to focus on the
framework or international consensus on how to develop patient, to societal changes and new research areas.
them in a standardised and evidence-based way.79,80 The This Commission is an international collaboration
generalisability of findings is also limited by the plethora between 30 experts in oncology, palliative care, public
of study designs, settings, and proposed pathways. This health, and psycho-oncology. In October 2016, a kick-off
situation makes the relevance of individual studies meeting was held in Milan, Italy, where panel leaders
difficult to evaluate and apply to clinical settings that are were appointed, the structure of the commission was
different from the one in which the specific SCP was decided, and a plan for the work was agreed on. During
developed and tested.81 In their review, Rotter and the 2 years that followed, each panel was expanded with
colleagues 7 assessed the effects of SCPs on professional experts within the relevant field, topical literature
practice, patient outcomes, and hospital costs. They searches were done, and experts participated in an
included 19 randomised trials comparing SCPs to interactive writing process. Both administrative and
standard practice, based on more than 3000 abstracts academic organisations were run, from Norway, by
identified in their search, covering a wide range of Stein Kaasa, Jon Håvard Loge, and Tonje Lundeby.
medical conditions and surgical procedures. Of the
included trials, nine gave some description of how the Policy—challenges and frameworks
SCP was developed and implemented. In those nine Demographic data show cancer incidence and prevalence
studies, the method applied to develop an SCP was are rapidly increasing, and that the population is ageing
mainly described in general terms—eg, a protocol was with multiple chronic comorbidities. A 2014 study83
developed by a multiprofessional team. Ten studies did a presenting various models for extrapolation in high-
follow-up on how health-care providers complied with income countries found that 69–82% of those who die
the SCP protocol, but none were done in a similar way. need palliative care. Consequently, an augmented need
Only one trial described how relevant clinical outcomes for palliative care at all health-care levels is expected.

Palliative care has been identified as an integrated part of Bismarck systems. Although the Beveridge system
the cancer care pathways by professional international seems to perform better in terms of care coordination
organisations such as ASCO, ESMO, and the European because health and social care are integrated in a
Association for Palliative Care (EAPC), but also by EU common welfare stem, this might only be the case at the
projects such as the European Partnership Against governmental level. In the Bismarck system, social and
Cancer.60,84–86 In sum, these statements indicate that other types of care (related to health but not necessarily
palliative care should be part of national cancer politics and inherent in health care) show a large degree of fragmen
plans.87 How this can be accomplished in present national tation because they are financed from different sources,
politics in Europe will be addressed in the following often as cash benefits or entitlements.
sections, where examples of different practices in At the 2011 conference for the Organisation for
organisation of palliative care in some European countries Economic Co-operation and Development,91 the sharp
and recommendations for future politics are given. distinction between these two systems was described as
mainly of historical interest, and the pure Bismarckian
Organisation and development of health policies and era as more or less over, because policies emphasised
systems universal coverage rather than a right of labour.
Health-care systems in Europe are generally classified with Furthermore, little, if any, scientific evidence for the
respect to the role of the state, health-care providers, and superiority of one system over the other exists, specifically
payers. This triad is furthermore amended by closer or regarding coordination of care, for which no universal
looser links with the social care sector. Countries with a definition presently exists.92 Palliative care has been
strong national health service tend to have closer links internationally acknowledged through a resolution by the
between health care and other sectors, including the social World Health Assembly.93
care sector. Health-care systems based on social health In Europe, the EAPC has, since its foundation, been
insurance systems have a looser link with the social care scientifically, clinically, socially, and politically influential
sector and, consequently, more often have gaps in the in the promotion, advocacy, and development of palliative
comprehensiveness and continuity of care. The type of care in Europe. In 2010, the EAPC launched the Prague
system is very relevant to palliative care, because the health charter,84 stating that access to palliative care is a legal
and social sectors often need to interact flexibly and quickly obligation and a human right, and thus beyond the
to meet the needs of the patient and family. established palliative care community. This charter was
Modern health-care systems in Europe build on the followed by the Lisbon challenge,94 identifying four major
experiences of the 20th century, when the state’s objectives related to access to essential medicines,
responsibility for delivery of health care became a social development of health policies that address the needs of
and political issue. This responsibility was primarily patients with life-limiting or terminal illnesses, adequate
approached in three different ways: the Bismarck palliative care training at undergraduate levels for health-
system,88 the Beveridge system,89 and the Semashko care providers, and a structured implementation of
system.90 The oldest of these systems, the social health palliative care. In 2013, the Budapest commitments
insurance system (Bismarck system), originated in presented frameworks for palliative care development as
1883.88 The coverage was gradually extended from a joint initiative by EAPC, the International Association
industrial workers to other categories of the workforce. for Hospice and Palliative Care (IAHPC),95 and the
In the 1940s, Lord Beveridge led the work on the Worldwide Palliative Care Alliance (WPCA).96 Key
development of the UK’s National Health Service,89 elements were policy, availability, education, and quality.97
which became a more comprehensive response to the In 2006, the European Palliative Care Research
demands for full coverage, irrespective of employment Collaborative (EPCRC) was the first palliative care
status (Beveridge system). Between these two systems is research project that received funding from the European
the Semashko system,90 which was developed in the Commission under the 6th framework programme for
1920s by the Soviet Union to deal with the organisational research. The promotion and financing of palliative care
aspects of health care, rather than financing or research within the EU framework was a major step
entitlements. forward for European palliative care research. Since then,
The main differences between the Beveridge and several high-quality projects on oncology and palliative
Bismarck systems are the degree of state control over care have received funding—eg, the IMPACT project, for
health care and how this control is exerted. In the the development and testing of quality indicators for
Beveridge system, the ministry of health is typically the dementia and cancer palliative care;98 EUROIMPACT,99 a
budget holder and therefore commissioning services multiprofessional research training programme; and,
through a network of health-care providers. In the the International Place of Death Study.100
Bismarck-type systems, budgets are predominantly with The objectives of the EU-funded PRISMA project
health insurance companies, regulated by the ministry of (7th Framework Programme) were to coordinate research
health and operating in public interest. The role of the priorities, measurement, and practice in end-of-life care
different partners has significantly more weight in in nine countries across Europe, resulting from an

identified need for high-quality palliative and end-of-life

Hospitals Outpatient Nursing homes Hospices Home care
care and research. The research agenda and subsequent clinic or day (and homes for
guidance should reflect the European cultural diversity care centres the elderly)
and be informed by public and clinical priorities.101 Belgium107 Y, PCU Y Y N Y
Consensus was reached on the following priorities for Bulgaria108 Y, including CCC N Y Y Y
end-of-life cancer care research in Europe: sympto and PCU
matology, issues related to care of the dying, policy and Denmark109 Y, including PCU N Y Y Y
organisation of services, and moving from descriptive to France110 Y, including PCU Y N N Y, including hospital
interventional studies.102 at home programme
Two EU-funded projects also addressing European Netherlands111 Y Y Y, including PCU Y Y
cancer politics have now come to an end: the European Norway112,113 Y Y Y N Y
Partnership on Action Against Cancer (EPAAC)103 and Slovenia114,115 Y Y N Y Y
the European Guide for Quality National Cancer Control Spain116,117 Y Y N N Y
Programs (CANCON).87 The EPAAC report on National
Y=provider available. PCU=palliative care units. N=provider unavailable. CCC=comprehensive cancer centres.
Cancer Plans (NCPs) was based on a survey running
from December, 2011, to April, 2012, in the EU Member Table 2: Providers of palliative care in some European countries
States, Iceland, and Norway.85 An NCP was defined as a
public health programme designed to reduce the number
of cancer cases and deaths, with strategies for key areas heterogeneity in the way in which national health
such as prevention, early detection, diagnosis, treatment, systems care for their dying, and in the quality and
rehabilitation, palliation, and research. The survey aimed access of the care provided, not only between countries,
to map the current level of integration in cancer care, but also within them.106 Countries involved in the
including palliative care, and to develop indicators to CANCON project have various policies on palliative
monitor the actions of NCPs across countries, before care. These policies are often nationally developed and
guidelines for the preparation or evaluation of cancer highly influenced by local opinion leaders in palliative
plans were developed. care; however, they do often refer to recommendations
The final EPAAC report points to significant variations for palliative care published by international organi
in cancer control and care within and between EU sations, such as WHO, the EU, or the Council of Europe.2
Member States across the key areas of cancer care Policies on horizontal and vertical integration of
mentioned earlier. The report identified that a compre services and structures for palliative care vary. Palliative
hensive approach was absent from policy documents care in Belgium, Bulgaria, Denmark, France, the
addressing the rising needs of patients with cancer, Netherlands, Norway, Slovenia, and Spain is provided in
especially because of the increasing incidence and various providers’ organisations and across all levels of
prevalence of cancer. Finland prioritised palliative care in care (table 2). Hospitals are mostly either specialised
its national cancer plan, whereas Estonia, Greece, and cancer centres or general hospitals authorised to parti
Portugal were without appropriate infrastructure to carry cipate in some or all parts of oncological care. Outpatient
out the NCPs adequately, especially with respect to home clinics might be organised as part of departments or as
care and palliative care services. This means that the special clinics for patients in need of palliative care. In
awareness of the need for palliative care is rising, but the many countries, nursing homes take over the care for
political willingness to dedicate adequate resources patients who, for various reasons, are not capable of
might be lacking. living in their homes.
The identified inadequacies in policy mentioned earlier In Belgium, France, the Netherlands, Norway, and
were included in the CANCON project, in which the Spain different types of networks and multidisciplinary
primary objective was to improve overall cancer control teams provide coordination or care, or both, at patients’
throughout the EU.87 The final guide covers the areas of homes, outpatient clinics, and in inpatient departments
quality-based cancer screening programmes, better in hospitals and nursing homes. The level of institu
integration of cancer care, community-based cancer care tionalisation seems to depend strongly on the specific
approaches, and survivorship. organisation of health care. Thus, in countries such as
The main target group for dissemination of CANCON Bulgaria and Belgium, the dependence on institutional
deliverables were policy makers and decision makers at care is great; whereas, in the Netherlands, palliative care
EU and national levels.104 Palliative care issues were is often primarily delivered in home settings by general
promoted as part of an overall disease trajectory, also practitioners and specially trained nurses.
pertaining to the primary care level.105 The compositions of the teams that deliver palliative
care vary across European countries. In the Netherlands,
European examples of organisation of palliative care a large proportion of palliative care is shouldered
The report by the European Parliament on Palliative by general practitioners, who—among others—run
Care in the European Union found a pronounced inpatient palliative care units in nursing homes. On the

other hand, in many countries palliative care remains a was founded. The Hospice Medicare Benefit Program
function carried out in hospital settings or in day was established by the Tax Equity and Fiscal Responsibility
hospital departments as part of hospitals. The hospital- Act in 1982, defining the payment and policies for
based palliative care policies are likely to become hospice care. By 2015, there were more than 5800 hospice
unsustainable either because of patient preferences, programmes across the country.
which indicate that patients prefer to be treated close to By contrast with community-based hospice programmes,
home when they need palliative care; or, because of the palliative care programmes reside in acute care facilities.
demographic changes that come with an increasing The first palliative care unit in the USA was established in
number of patients needing palliative care, which the Cleveland Clinic in 1988. Over time, other cancer
cannot realistically all be organised in hospital settings centres have developed models of excellence for integrated
alone. palliative cancer care, such as the MD Anderson Cancer
Although palliative care in European countries is Center.7 Since the 1990s, the proportion of cancer centres
delivered in different settings, it is difficult to identify a with outpatient clinics to facilitate timely palliative care has
systematic pattern based on the health-care system in the grown.119,120 In 2006, the American Board of Medical
country. This observation confirms the hypothesis that Specialities recognised hospice and palliative medicine as
palliative care is underdeveloped in the health-care a medical specialty, further promoting the growth of this
system, and is too dependent on individual initiatives. discipline.
From the project meetings and interviews that formed
part of the CANCON project, it became evident that in Australian policies on palliative cancer care
the Netherlands, a patient with a condition that requires Palliative care has had growing recognition in Australia
only palliative or end-of-life care, or both, is discharged over the past three decades. The subspecialty was first
from inpatient oncological facility and their general recognised within the College of Physicians in 1988,
practitioner and district nurse informed. Some of the when training also became available. Specific national
patients who cannot stay and be cared for at home are policies allowing reimbursement for clinical care were
placed in nursing homes with palliative care units, which introduced in 2000.
are run by general practitioners trained in palliative care. A national strategy has been endorsed by all states and
In many countries, this would not meet the patient’s or territories since 2000. This strategy sought to address
family’s expectations. This is in contrast with the access and equity, models of care, and the relationship
Bulgarian system, where cancer care is exclusively between specialist services and the rest of the health
delivered by the so-called Comprehensive Cancer sector, including primary care. The strategy has been
Centres, which exist in all regions. revised twice since its genesis, and has had com
When comparing the analyses of EU and EEA prehensive evaluations for its first two iterations.121
countries’ cancer plans in 2011, and 2016, we observe a
trend towards more frequently including palliative care Approaches for integration of cancer and palliative care
as an element of the cancer plans. In most cases, Coordination of care, regardless of definition, is demand
palliative care is regarded as an add-on service, receiving ing, involves a vast number of professionals, and multiple
less attention than the traditional diagnostic and transitions from one care level to another throughout the
therapeutic elements of cancer care. disease trajectory, which makes colla boration and inte
Barriers to integration of palliative care into a compre gration of services paramount. One response to this
hensive plan seem to fall into two clusters. One is the complex process is the introduction of standardised care
fact that health systems have different traditional and pathways, which have been adopted and adapted to cancer
current attitudes with respect to palliative care, which care in several countries (eg, Belgium, France, the
impedes a more open debate on how to organise, place, Netherlands, Norway, and Spain).
and staff palliative care as an element of a continuous Another organisational principle, focused at an even
cancer care. The other cluster seems to be a lack of more granular level, is multidisciplinary teams. The idea
commitment from decision makers or reimbursement of multidisciplinary teams was proposed by an EPAAC
agencies, or both, to secure financial resources and working group as a core element for an effective
organisation capacity that make palliative care accessible European cancer care policy. From this proposal, a policy
to all patients who need it irrespective of their financial statement122 on multidisciplinary cancer care was
ability to pay for care. formulated for implementation by all tumour-based
multidisciplinary teams, to provide patients with the care
US policies on palliative cancer care they need. The multidisciplinary teams might be a place
Palliative care was introduced to the USA in 1963.118 It for integration of palliative care through an assessment
started as a hospice movement, focusing on the provision of, and discussion about, patient-centred needs at any
of home-based care to patients in the last weeks or days stage of the disease trajectory. The policy statement is
of life. In 1973, the first hospice was established in intended to serve as a reference for policy makers and
Connecticut. In 1978, the National Hospice Organization health-care providers to improve coordination.

The ASCO recommendations123 for early referrals to

specialist palliative care teams, and the other listed Panel 2: Requirements for collaboration between
policy statements on integration of cancer care and oncological specialists and primary care doctors
palliative care, conflict with the documented workforce • Definition of when end-of-life care begins
shortage in palliative care.124 Thus, it is necessary to • Assessments of the patterns and specific components of
define the level of palliative care expertise at all health- end-of-life care as provided by different types of
care levels, be it in tertiary specialist centres or home oncologists and primary care physicians
care (see later sections of this Commission on models of • Understanding of patient and caregiver preferences for
palliative care integration and the role of education). the relative involvement of oncology versus primary care
Oncologists, palliative care specialists, and other medical specialists at the end of life
relevant health-care professionals should be part of all • Design of appropriate and validated assessment tools to
hospital SCPs, whereas primary care workers must have further understand how end-of-life care should best be
basic palliative care skills to meet patients’ needs. managed
However, an Australian survey125 reported that a • Evaluation of the effect, in terms of quality of care and
substantial number of general practitioners (31%) felt other endpoints, of different models of end-of-life care
they had inadequate training and insufficient resources and understand how these different models might be
to provide home-based care to patients with advanced implemented in different health-care delivery systems
cancer, which is a challenge to be addressed by • Ascertainment of best practices and methodologies for
educational programmes (see later section of this the integration of primary and oncology specialty care in
Commission on education). patients dying of advanced cancer
The gap between hospital-based SCPs and the primary
care level is well known, but challenging to fill because of
differences in funding and administrative allocation. In but rather on defining, or redefining, the care pathways of
practice, this gap is often compensated for by informal patients with cancer to map all services required to meet
networks. Bainbridge and colleagues126 explored the patients’ needs throughout the disease trajectory and
horizontal integration among professionals in informal beyond. This means that cancer patients and in particular,
palliative care networks. They found that these informal cancer survivors, need support and management of their
networks often produced positive results and were health issues and challenges beyond the curative phase.
well accepted, but interprofessional communication Such efforts will often involve their families and other
and evaluative activities were commonly perceived as sectors of the society. A 2018 Canadian study130 showed
insufficient. Han and Rayson127 explored the collaboration that citizens’ expectations are high with respect to the
between oncological specialists and primary care doctors integration of palliative care standards into the Canada
and their roles in the end-of-life care, and concluded that Health Act, and thus into the basic processes of care. The
further elaboration, reflection, and research was required survey showed that there are clear concerns around the
(panel 2). financial accessibility of such care, but this is regarded as
The disease trajectory of a patient with advanced cancer a condition for successful implementation of such a
consists of several subpathways, and many patients will programme. The majority of Canadians agree that surveys
be in an incurable state for many years, with large should be done among family members (84%), caregivers
variations in the need for palliative care. During these (82%), and patients (79%) regarding the care received, and
years, several transitions of life expectancy will occur, all 72% of Canadians agree that annual surveys should be
of which present multiple challenges and complaints done to measure and track Canadians’ level of awareness
related to insufficient communication across care levels, of palliative care.130 At the political level, these findings
fragmented care, and unclear responsibilities. Thus, we support the obligation for politicians and health authorities
recommend that assessment of patient preferences and to put palliative care on the agenda as an integrated part of
planning of transitions should be focused in early the health-care system, and not as a so-called hidden
palliative care consultations, as should the use of SDM as service for dying patients.
part of the SCPs. This seems pertinent, given that 82% of
late palliative care (<90 days before death), as reported in Costs and cost-effectiveness of palliative care
a study by Scibetta and colleagues,128 was for end-of-life Major concerns in oncology today are the rapidly
admission to hospital, or that only 8% of patients with increasing complexity of treatment and costs of care,
lung cancer in the USA see a palliative care specialist, which threaten the sustainability of the present
often to address end-of-life issues.129 As a rule, a patient’s services.22,131 As pointed out by Isenberg and colleagues,123
needs should be assessed as a continuous process from increased delivery of palliative care, as recommended by
diagnosis onwards, and palliative care needs should not the updated ASCO guidelines,15 must be accompanied by
be an exception to this rule. changes in the financing of health care.
The work in the CANCON project, therefore, did not An editorial in the Journal of Oncology Practice132
focus on one particular aspect of cancer care in isolation, concludes that the determination of cost-effective

methods to care for patients with advanced cancer should Larger and sufficiently powered cost studies showing
be given high priority, based on the rapidly increasing that these additional costs offset savings in other domains
demand for palliative care in an ageing population. of oncology and end-of-life care are needed. Greer and
However, valid methods for cost estimates that consider colleagues149 analysed cost data from Temel and colleagues’
both cost-effectiveness and cost-benefit analyses (out study,3 and found that patients in the early palliative care
comes translated to money) need to be established. group had higher hospice costs, but lower costs related to
Although palliative care interventions have been shown chemotherapy in the last 30 days of life than patients in
to improve patient-reported outcomes3,5,56,133–136 and cut the control group. Some studies have examined the cost-
costs for second party payers and hospitals,137–139 most effectiveness of specialised palliative care, and report
studies are small and are done from the health services diverging results. This divergence is mainly related to
perspective, not the societal perspective.132 Thus, they differences in financial incentives and reimbursement
often do not include patient, caregiver, and societal costs issues, whether patients are seen exclusively on an
in the calculations. outpatient basis, if the unit is located together with other
Intensive end-of-life care is expensive, but studies highly specialised teams providing palliative care services,
fully illuminating the costs associated with integration and referral and follow-up practice. Referral and follow-
of oncology and palliative care are in short supply. There up practices will be an important and political issue in the
are findings that indicate integration is more cost- years to come, as an increasing amount of palliative care
effective than standard treatment. Early palliative must be delivered by primary health-care services. As
referrals improve end-of-life care in terms of earlier pointed out previously, the need for care delivery at this
hospice referrals,140,141 lower readmission rates to level has implications for the education of primary health-
hospitals,142 and shorter length of hospital stay,143 care personnel (see the section of this Commission on
contributing to substantial reductions in cost. According the role of education). Systematic palliative care
to Cassel and colleagues,144 early palliative care is an interventions initiated at the specialist levels, but also
excellent example of how to improve or maintain quality followed by multidisciplinary palliative care teams, have
of health-care delivery for patients and caregivers at a improved patient-reported outcomes and proven cost-
lower cost. Furthermore, most costs in late-stage cancer effective.150–152 The 2017 book by Gómez-Batiste and
have been shown to result from advanced therapy with Connor153 states in its general conclusion, based on global
marginal effects, intensive care unit and emergency data, that home and community-based services are
admissions, and protracted hospital stays, rather than emphasised over building inpatient palliative services.
from direct personnel costs.145 Estimates from the USA Researchers have started examining a quantifiable, or at
and UK indicate 25% of health-care expenditure is least a qualitatively comparable, contribution of the
related to patients in their last year of life, whereas end- different models in palliative care. An example of such a
of-life care takes up 20% of hospital beds.146,147 In sum, study is that by Siouta and colleagues154 from 2016; the
these figures and findings indicate expenditures that authors did a qualitative systematic literature review of
can be reduced, and that integration can serve this empirically tested models in cancer and other chronic
function. diseases, including 14 studies, seven models for chronic
The present evidence of better care at lower costs disease, four for integrated care in oncology, two for both
associated with early access to palliative care makes it cancer and chronic disease, and two for end-of-life
necessary to evaluate the policy on subsidies, revenues, pathways. The involvement of a palliative care multi
payment for patients, reimbursement practice, and disciplinary team resulted in better symptom control, less
organisation of services to promote integration of caregiver burden, improvement in continuity and
oncology and palliative care. Although copayment for coordination of care, fewer admissions to hospital, cost-
patients might be one option to promote integration, it effectiveness, and more patients dying in their preferred
might be unacceptable from a societal point of view place. The authors proposed a generic frame work for
because underserved populations might refrain from integrated palliative care in cancer and chronic disease.
using the service. Compulsory palliative care consul This framework promotes the integration of palliative
tations alongside tumour-directed treatment at a certain care in the disease trajectory concurrently with disease-
stage of advanced disease is another option; however, use oriented treatment, and the employment of a palliative
of a time-based model, as compared with a patient- care-trained multidisciplinary team with a three-fold
centric, need-based model,148 adds cost to the already focus: treatment, consulting, and training.
substantial cost to this group of patients. This added cost Few resources, pressures on cost containment, cost-
primarily relates to personnel costs at the tertiary level; effectiveness, and overall cost control are present in
eg, consultations with both oncologists and palliative cancer care, as well as in palliative care; consequently, it
care specialists, and more time allocated to the is necessary to look at the best performing types of care
consultations. Another option is to make reimbursement in the whole cancer care trajectory. Smith and colleagues137
conditional on palliative care involvement at a certain did a comprehensive review of available international
stage in the disease trajectory.123 evidence on the cost and cost-effectiveness of palliative

care in any setting (hospital based, home care, or hospice and structures within society and the normal patterns
based). The quality of retrieved papers was assessed of practice. Societies are comprised of many different
against 31 indicators developed for the purpose of their communities, in turn comprised of many different
review. The authors identified 46 papers meeting the groups of people; any issues associated with these
inclusion criteria; from these they found that palliative groups can be described as societal. In this section, we
care is very often less costly relative to the comparator consider the challenges at societal, professional,
groups and, in most cases, the difference was statistically patient, public, media, and medical education levels
significant. that could hamper the better integration of palliative
Standards, guidelines, and guidance are meant to care and oncology.
standardise procedures, and SCPs can be used as an
implementation tool to equalise quality and enable Professional: oncologists, palliative care, surgeons,
comparative analysis in health care. As much as SCPs are general medicine, and primary care
helpful, at the political level they might cause tension and Although much practice by oncologists involves people
frustration related to struggles to secure adequate human with advanced cancer, and despite recommendations by
and financial resources. However, if a country’s goal is to ESMO155,156 and the Organisation of European Cancer
deliver high-quality cancer care, these tensions and Institutes157 that, to be designated, a cancer centre must
frustrations need to be addressed, and directions need to have integrated oncology and palliative care, the liaison
be given by the governments based on a sustainable and integration of oncology with palliative care varies
health policy and independent of who is in power. This considerably.
approach is strongly supported by all international A survey158 of 895 members of ESMO from 64 countries,
statements that access to palliative care is a human right. including 34 in Europe, regarding their involvement in
Given the challenges facing patients, care providers, and attitudes toward the palliative care of patients with
and the system as a whole, the bulk of financing should advanced cancer, found that although the importance of
come from public funds, or, at least, the share of public
financing dedicated to palliative care should not be
different from the financing of other health-care services Panel 3: Policy—recommendations
within a given system. To raise the profile of palliative Barriers
care at the political level, the following arguments could • Palliative care not perceived as a needed integral part of the cancer care continuum
be made: (1) the needs for palliative care are rising, and • Deficient planning of palliative care at national and regional levels
many present needs are unmet; (2) palliative care is part • Insufficient organisational and infrastructural capacity of palliative care
of the cancer care continuum; (3) palliative care is patient • Palliative care limited to respite care and supportive care, and often left to the family
centred and should be delivered systematically; (4) SCPs • Inadequate assessment of costs and benefits of palliative care
can secure availability of palliative care, but presupposes
relevant professionalism at all levels, and willingness and Solutions
resources for the implementation; (5) the population is • Establishment of standardised care pathways that cover all cancer care services
fragile, does not demand expensive treatments, but is (envisaged also by National Cancer Control Programs)
without public representatives; (6) the industry or other • Adherence to the European Guide for Quality of National Cancer Control Programs
key stakeholders with easy access to the political • The need to invest in palliative care infrastructure—partly related to the workforce
decision-making processes are focused on treatments • Build on infrastructure for palliative care also in outpatient and home settings to
other than palliative care; and (7) the fragility of both address the needs of cancer patients
patients in need of palliative care and their relatives • Transparency of direct and indirect costs, and also doing health technology
incapacitates them in the public debate on resource assessment for palliative care procedures
allocation, and public funding is therefore necessary. The Recommendations for immediate action
main question is: how can we ensure policies on palliative In order to develop better integration of oncology and palliative care, WHO and
care are effectively implemented? Concerted action of professional organisations (European Association of Palliative Care [EAPC], Worldwide
cancer care professionals and patients, through advocacy Palliative Care Alliance [WPCA], International Association for Hospice and Palliative Care
efforts, is needed; specifically, a case needs to be made for [IAHPC], European Oncology Nursing Society [EONS], European Society for Radiotherapy
the currently unmet needs that place a significant burden and Oncology [ESTRO] and American Society of Clinical Oncology [ASCO], among others)
on the individual, family, health care, and, ultimately, on should work together to establish consensus on structure and implementation plans to
society as a whole (panel 3). guide policy makers based on present best knowledge for the following areas:
• Convergent policies worldwide addressing integration of oncology and palliative care
Societal challenges • Organisational structures of early integration of oncology and palliative care in
Despite the growing evidence for the benefits of hospitals
integration of palliative care and oncology for patients • Organisational structure of early integration and collaboration between hospitals and
and those close to them and to health-care systems, community care in oncology or palliative care, or both, at global level need to be
many challenges remain. Some of the challenges can developed
be considered societal; ie, problems in the interactions

palliative care was recognised, actual participation levels qualitative in-depth interview study176 in Germany found
are suboptimal. 43% of respondents reported that they that oncologists reported patients with unrealistic
directly administered end-of-life care often, and 74% expectations to be a challenge for end-of-life
reported that they derived satisfaction from their communication, especially in comprehensive cancer
involvement in end-of-life care. Only around a third of centres. Oncologists responded to this challenge quite
respondents often collaborated with a palliative care differently, by either proactively trying to facilitate
specialist (35%), a palliative home care service (38%), an advance care planning or passively leaving the initiative
inpatient hospice (26%), or a psychologist (33%). Yet, to address preferences for care at the end of life to the
respondents were more commonly involved in treating patient. A major impediment to the proactive approach
physical symptoms (eg, pain [93%], fatigue [84%], and was uncertainty about the right timing for end-of-life
nausea or emesis, or both [84%]), than in managing discussions, and about balancing the medical evidence
psychological symptoms and end-of-life care issues against the physician’s own subjective emotional
(eg, depression or anxiety, or both [65%], existential involvement and the patient’s wishes. These findings
distress [29%], or delirium [12%]). Most respondents might help to explain why end-of-life communication is
(88%) endorsed the belief that medical oncologists often started rather late with patients with cancer.
should coordinate the end-of-life care for their patients Uncertainty in prognosis and likely treatment out
with cancer, but almost half (42%) said they felt they were comes is inevitable in complex illnesses with evolving
trained inadequately for this task. Although most of the treatments, like cancer. In modern times, with increas
responding medical oncologists expressed positive views ingly intensive treatments and population ageing, more
regarding their involvement in the palliative care of people face more complex treatment, care decisions, and
patients with advanced cancer and patients who were uncertainty.177 Uncertainty can become a major barrier to
dying, 15% of respondents had pervasively negative effective care because clinicians delay raising issues or
views.158 Similar challenges have been reported among making decisions in an attempt to reassure in the face of
oncologists in other countries, including China, uncertainty.178 A study177 of decision-making processes
Thailand, USA, and many others.159–169 during critical care found that decisions were made
Oncologists’ end-of-life care attitudes can influence serially, over the whole disease trajectory, which usually
their timely palliative care referral and end-of-life cancer covered several days or weeks. Four trajectories with
treatment decisions. Oncologists often refer patients to distinct patterns were identified: curative care from
palliative care late in the course of illness,163,164,170–173 despite admission; oscillating curative and comfort care; shift to
believing—as found in recent surveys170,173—that inte comfort care; and comfort care from admission. Conflict
gration of early specialist palliative care in cancer between patients and clinical teams and within clinical
improves symptom control, end-of-life care, health- teams occurred most commonly in the trajectories with
related communication, and continuity of care. A oscillating curative and comfort care. This complex web
survey174 of 182 oncologists from a major cancer centre in of discussions means early communication is needed,
the USA found that comfort with the concepts of end-of- especially around the values and preferred care outcomes
life care was associated with higher rates of specialist from care of patients and their families. The study also
palliative care referral and self-reported primary palliative suggested there should be clearer discussions of
care delivery. A 2015 systematic review52 found that the treatment plans, rather than waiting until the end of life.
definitions of the concepts of integration varied. A further issue impeding integration might be the
In many instances, decisions against intensive treat research focus of oncology versus that in palliative care.
ments are often made only when death is imminent. A Only a tiny proportion of research spending in cancer is
study175 in which Belgian oncologists were interviewed allocated to palliative or end-of-life care, by contrast with
identified seven categories of barriers that discouraged that spent on studying oncological treatment. Data on
oncologists from discussing palliative care: oncologist- research funding by National Cancer Research Institute
related; patient-related; family-related; barriers relating partners in the UK, based on studies included in the
to the physician referring the patient to the medical National Cancer Research Database for 2015–16, found
oncologist; barriers relating to disease or treatment; that, of the £579·79 million awarded for research into
institutional or organisational barriers, or both; and cancer, just 0·33% (£1 925 909) was allocated to palliative
societal or policy barriers, or both. Communication, and end-of-life care. By contrast, £207·28 million
approaches to the management of uncertainty in illness, (36%) was allocated to research into treatment, and
and broader cultures and the focus of research in £163·11 million (28%) to research into the biology of
oncology might play a role here. Sympathetic, yet honest, cancer.179 This small amount is often spent across
communication about the irreversible nature of advanced multiple projects, meaning that the support for
cancer is important to improve patients’ prognostic evaluative trials, or new palliative treatments, is
under standing and, thereby, to allow for treatment insufficient.
intensity to be adjusted to realistic goals, and to overcome These figures are similar to those reported for 2010,
some of the patient-related and family-related barriers. A when only 0·24% of cancer research spending in the UK

went to palliative or end-of-life care, although the overall World Health Assembly, when WHO passed the first
funding for research in cancer increased slightly.180 resolution on palliative care, recommending national
Similarly, in the USA, of the National Cancer Institute’s health systems provide palliative care in conjunction
total appropriation for 2010 of US$5 billion, only 1% was with potentially curative treatment, and not just as an
awarded to palliative care research.180 Data in Australia optional extra.185 The resolution urged Member States to
mirror these findings, although, on a positive note, the develop and implement policies that support the
Australasian Clinical Oncology Research Development integration of cost-effective and equitable palliative care
programme specifically seeks to attract young clinical services in the continuum of care, across all levels.186 A
palliative care researchers to develop their clinical trial modern approach to palliative care can also include an
protocols alongside young oncology trainees. This focus integration with oncology and relevant community and
on research on treatment might further drive oncologists hospital services.187
towards tumour-directed treatment and in valuing cure
over improving quality of life and palliative care. Patients, families, the public, and the role of the media
Opportunities for oncologists to develop in teaching Public priorities when faced with a terminal illness, such
hospitals, with a combined career in research and practice, as an advanced cancer, would suggest that better
are therefore almost exclusively in the area of cancer integration of oncology and palliative care is important
biology or cancer treatments and almost never in palliative for care and would be preferred. A population-based
care, where the funding for individual projects seems to be survey188 of people’s priorities for treatment, care, and
insufficient to support a substantial fellowship for a PhD information across seven European countries asked
or MD. Investment in research into palliative and end-of- respondents for their priorities if faced with a serious
life care is urgently required to inform the transition from illness, like cancer, with limited time to live. Of the
tumour-directed care to palliative care, improve symptom 9344 individuals interviewed, most people (57% [Italy] to
control, deliver cost effective care, and ensure that choices 81% [Spain]) would choose to improve quality of life for
at the end of life are offered and met; in turn, this will help the time they had left. Only 2% (England) to 6%
to further the integration of palliative and oncological care. (Flanders) said extending life was most important. An
There are some proposals that palliative care would be important minority (15% [Spain] to 40% [Italy]) said
more acceptable to oncologists if it were renamed quality and extension were equally important.
supportive care.181,182 However, others have argued that Prioritisation of quality of life was associated with higher
any proposed renaming clouds the more nuanced issues, education in all countries. The survey included people
such as attitudes and resources, and the issues raised with different health statuses, but these did not affect
earlier, which together hamper referrals.183 Supportive priorities. Further components of this survey in the
care is something that all oncologists should do, and the open-ended questions identified a public perception of
term is much linked to cancer. Others have proposed needs for improved quality of end-of-life and palliative
renaming palliative care as enhanced supportive care. care and access to this care for patients and families, and
The important questions, however, should be around a recognition of the importance of death and dying, the
what patients and families feel are appropriate services, cessation of treatments to extend life unnecessarily, and
not what professionals feel they would like to refer to the need for holistic care to include comfort and
when discussing their service. support.189 Most people would want to know if they had a
A further consideration is the attitudes of palliative terminal illness, and factors associated with this wish
care to oncology. Palliative care services are overstretched, have been identified.190
with staff shortages and insufficient resources to treat all Public awareness of palliative care and related services
patients. They are often supported by the charitable among oncology patients is often scarce. One survey,191
sector, and, in many countries, are not included in done in London, UK, found that only 19% of patients
mainstream health-care funding. These factors can lead recognised the term palliative care, although 68%
to services being limiting. The US hospice benefit, understood the role of the hospice, and 67% understood
which reimbursed the provision of hospice care under the role of Macmillan nurses (specialist nurses providing
Medicare, included the stipulation that patients should an advisory palliative care service in the UK). Age-
have a prognosis of 6 months or less, and that patients in adjusted multiple logistic regression found that the most
hospices should agree to withdraw from all treatment of socially and materially affluent patients were eight times
potential curative intent.184 Although this definition does more likely to recognise the term palliative care,
not exist in most countries outside the USA, the earlier compared with those who were the poorest. A survey192 in
focus on palliative care at the end of life can limit Japan found similar challenges in awareness of palliative
referrals. Palliative and oncology clinicians have to care. In 2017, an internet search query193 in the USA
recognise the change in the needs of patients with found that public awareness of the term palliative care is
cancer; specifically, the need for earlier, more integrated growing month by month.
care as a consequence of changes in treatment and Uncertainty around decision making and difficulty with
disease trajectory. This was clearly expressed at the 67th communication are also likely to have a role in hampering

the integration of palliative and oncology care for patients difficulty in communication, and create stigma associated
with cancer during treatment. In a qualitative study177 of with accepting anything not directed towards cure.
intensive care, uncertainty was a pervading feature over Public communication is probably crucial to decrease
the trajectory of care. Families were most often involved in cancer-related and palliative care-related stigma, raise
decision making regarding care outcomes, and seemed to awareness, disseminate education, and direct patient and
find it easier when patients switched definitively from family care.211,212 Wide-ranging public education; links to
curative to comfort care. Some families considered schools; use of modern forms of media, such as social
decision making a negative concept, and preferred media; use of web-based media for better information
uncertainty. We found eight categories of decision about cancer care and palliative care;213 and more
making: three related to the care outcomes (aim, place, traditional health education are needed.214 Cultural
and response to needs) and five to the care differences in beliefs in, and response to, cancer,
processes (resuscitation, decision support, medications/ palliative care, information needs, and end-of-life care
fluids, monitoring/interventions, and other specialty need to be respected and accounted for in this
involvement). The study suggests a need to support early communication process.215
communication, especially around values and preferred Despite the fact that cancer is a major and increasing
care outcomes, from which other decisions follow, health problem, particularly in older people, paradoxically,
including “do not attempt to resuscitate” decisions. Simple older people with cancer are often undertreated when
tools to understand patients’ and families’ priorities and compared with younger patients, and are excluded from
aid communication have been developed and undergone clinical trials.216 The inequalities do not only pervade new
preliminary testing, with many promising to improve this therapies, but also reconstruction surgery, nursing,
situation.194 primary, and palliative care—eg, immunotherapy, breast
Stigma surrounding cancer is common, and presents a reconstruction, and chemotherapy rates are lower for
great challenge to treatment and care,195–197 including to older patients than for younger patients. In one study,217
palliative care and its integration with oncology. Stigma nurses’ visions of ageing influenced reduced support for
can have a silencing effect. The social, emotional, and breast reconstruction: nurses with a negative view of age
financial devastation that all too often accompanies a discriminated against a 75-year-old patient more than a
diagnosis of cancer is, in large part, due to the cultural 35-year-old patient (ie, less encouragement was given to
myths and taboos surrounding the disease.195–197 There are the older patient). Older patients have less access to
several reasons that cancer and, within this, palliative inpatient hospice and palliative care services than
care might be stigmatised.198,199 Symptoms or body parts younger patients, although this seems to be improving
affected by cancer can cultivate stigma, as can beliefs slightly.218 Older people are more likely to die in hospital
about treatment.200 Pain, other symptoms, or the cancer and less likely to die at home, which is often their
itself can be seen as a test or punishment, affecting preferred place of death, when compared with younger
the willingness to use therapies or to be referred to patients.219 A large population-based study220 found that
palliative care.201 Breathlessness and cough are common older patients with lung cancer (aged >60 years) had
symptoms, but are associated with social withdrawal, significantly lower chances of receiving opioids than
non-response of services, and invisibility.202,203 Depression their younger (aged <50 years) peers (prevalence ratio
is a stigmatising symptom in many countries.204 Negative range, 0·14–0·78), even adjusted for comorbidity.
illness perceptions can increase depression.205 Some
cancers or their treatment cause changes in appearance, Barriers and challenges related to death and dying
which can also be distressing and result in stigma.206 Fear Death and dying are often taboo subjects associated
of dying and the stigma associated with terminal events with considerable stigma for people who are dying and
might also hamper access to palliative care.207 Although those close to them. This is a challenge at a professional
many people report that they grow despite cancer, level, patient and caregiver level, and a societal level. A
treatment, and through stigma, appropriate support study221 of 233 college students used a range of semantic
systems and resilience are needed.206 differential adjectives to explore their attitudes toward
News reports about cancer frequently discuss intensive young and old people who were healthy, ill, or terminally
treatment and survival, but rarely treatment failure, ill. The results identified negative attitudes toward
adverse events, end-of-life care, or death.208,209 These dying people in both young and old age groups; their
portrayals of cancer care might give patients an role was conceptualised as undervalued, indicating
inappropriately optimistic view of cancer treatment, stigma towards those who are terminally ill. Saunders222
outcomes, and prognosis. Language in the media wrote on the need to change this stigma, and focus on
likening cancer to a battle or war and conflating cancer living and dying well. Writing in The Lancet in 1984,
and fear210 might lead people whose disease is continuing Wilkes223 drew attention to the challenges that such
despite treatment to feel like a failure (ie, that they are stigma brings.
losing the war) and become reluctant to seek or discuss Stigma and taboo still pervade society, leading some
any alternative. All of these factors might result in countries to launch education campaigns in response—

eg, the UK’s Dying Matters initiative.224 Because death has 53% of cancer deaths occur in countries at a low or
become less common in our daily lives, it has possibly medium level of the Human Development Index.236
become harder to consider our own mortality, or that of Projections suggest that if the cancer-specific and sex-
those close to us. Some researchers and clinicians have specific trends estimated in this study237 continue, the
said that there is neglect within oncology with regards to incidence of all cancer cases will increase from
patients who are dying. This might be a particular 12·7 million new cases in 2008 to 22·2 million by 2030.238
problem in oncology, and sometimes in cancer nursing, This affects all countries, with an increase of 68%
where the focus is on more treatment, on cure, and on compared with 2012 overall, and 66% in low and medium
fighting the illness, rather than on living and dying well.225 Human Development Index countries and 56% in high
The emphasis on cure might be helpful when encouraging and very high Human Development Index countries.238
patients to come forward for screening or early Although early resolutions regarding palliative care
treatment,226,227 but there are many examples of patients mainly focused on the more advanced stages of disease
receiving chemotherapy in the last 30 days of life, when it and the end of life,29 the WHO mandate on palliative care
is not thought to be effective.228 Death often remains a has been extended to include patients in the early phase of
taboo subject in the clinical encounter.229 An absence of all diseases. This evolution of the WHO mandate reflects
openness about death has negative consequences for the the evolution of the concept of palliative care as a whole,239
quality of care provided to the dying and bereaved, with which consists of extension of care beyond cancer and
missed opportunities for symptom management and into more general chronic conditions, promotion of early
psychosocial support.222 Lack of honest disclosure is seen palliative interventions in the clinical evolution of the
along the disease trajectory, from time of primary disease, application of palliative care measures in all
diagnosis to relapse and terminal illness. This prevents settings of the health-care system, and identification of
patients and families to reorganise and adapt their lives to complexity versus prognosis as criteria for specialist
the present situation.230 interventions. In other words, the focus of palliative care
An absence of openness often pervades undergraduate has shifted from the concept of terminal illness to
and postgraduate medical education, including specialist advanced chronic illness with a limited prognosis, and
training in oncology, in which many doctors and from a specialty approach to a national health-care system
students feel unprepared to discuss death and dying, approach.29,240 Recommendations are presented in panel 4.
deteriorating illness or even to break the news of a death
to family members and friends.231,232 Failure to have those Prognostication
conversations can deny patients and families the The importance of prognosticating in oncology and
opportunity to make important decisions.230 These are palliative care
difficult conversations; some might not want to talk Prognostication is the skill of predicting future outcomes.
about the end of their life, and others might want to talk, The outcome that is most commonly predicted is the
but at different times and stages. It is often difficult to duration of patient survival, although one can also
know how to open these conversations, but there is prognosticate about other clinically relevant outcomes,
evidence that through training and continued support it such as symptomatic response to palliative treatment,
can be done, even in the context of offering further discharge from hospital, or recovery of function. Once
treatment.233–235 Tools have been developed to help
clinicians to ask about and understand patient priorities,
and these could be a starting point for dialogue.194 Panel 4: Societal challenges—recommendations
• Encourage public actions that focus on death as a part of being human by
Implications developing international and national consensus programmes (campaigns) on
Cancer is one of the most common health issues in being mortal; and engaging in the international and national parliaments, patient
society. Worldwide, 14·1 million new cases and organisations, and professional organisation campaigns
8·2 million deaths from cancer were reported in 2012. • Destigmatise palliative care by developing international and national consensus
The most commonly diagnosed cancers were lung cancer programmes and engaging parliaments, patient organisations, and professional
(1·82 million), breast cancer (1·67 million), and colorectal organisations in the campaigns
cancer (1·36 million); the most common causes of cancer • Ensure economic resources to palliative care and palliative care research reflect the
death were lung cancer (1·6 million deaths), liver cancer needs and the volume of the patients in oncology practice by establishing an
(745 000 deaths), and stomach cancer (723 000 deaths).236 international expert panel to develop multinational estimations of needs, reflecting
The Global Burden of cancer analysis from 2008, showed the complexity of the patient population
that an estimated 169·3 million years of healthy life were • Raise public awareness of the goals of tumour-directed treatment (life-prolonging,
lost to cancer that year.237 Colorectal, lung, breast, and symptomatic, and end-of-life care) by starting international and national
prostate cancers are the main contributors to total years discussions on information policies and communication in the public domains
of life lost in most world regions, and caused 18–50% of aiming to raise awareness of the marketing by the medical industry and health-care
the total cancer burden.237 Cancer will increase in all parts providers
of the globe. Currently, around 44% of cancer cases and

patients have received an accurate diagnosis of cancer, the common.251–253 In one study,253 only 108 of 216 patients
next question is frequently about the likely prognosis.241 correctly identified whether the treatment they were
Oncologists are routinely required to prognosticate. At receiving was curative or palliative in intent. Similarly, in
diagnosis, prognostication primarily relies on an accurate another study,254 64% of patients with incurable lung
staging of the extent of disease. All cancer staging cancer did not report understanding that their
systems are based on the premise that the severity and radiotherapy was unlikely to cure them. This mismatch
extent of disease is associated with different outcomes between clinicians’ and patients’ understanding about
(particularly the risk of death). At diagnosis, the stage of the indications for their treatment is not confined to
disease frequently dictates the preferred course of oncologists. In a 2015 study,255 57·4% of patients with
treatment. Detailed prognostic information about sur metastatic lung, and 79·8% of patients with metastatic
vival associated with each stage of disease can help colorectal cancer believed that their surgery was likely to
patients and clinicians to make informed decisions about have been curative. Moreover, evidence exists that
the best course of treatment. patients with advanced cancer are subject to increasing
In palliative care practice, the issue of prognosis is also numbers of radiological investigations,256 and to a higher
very important, although, in these circumstances, the frequency of investigations when they are closer to death,
question is more specifically about how long patients are and of artificial nutritional support, even in the context of
expected to live, rather than on predicting their response decreased SACT.257
to further treatment.242 In routine practice, issues of
prognosis are pertinent to decisions and discussions Predicting survival in advanced cancer using prognostic
about place of care, advance care planning, and tools
determining ceilings of care.243–245 Accurate staging can provide valuable prognostic
At the interface of oncology and palliative care, information, guide decision making about treatments
prognostic questions are most relevant to the decision at the individual patient level, allow for a common
about whether or not to proceed with palliative international terminology so that different centres can
chemotherapy. Deaths occurring within 30 days of accurately describe the case-mix of their patients and
chemotherapy are increasingly recognised as an indicator compare outcomes, and is essential for the identification
of the quality of oncological care.246 When used of homogeneous populations for entry into clinical
appropriately, palliative chemotherapy can improve trials.258 However, in the context of palliative care, when
quality of life and survival in patients with advanced nearly all patients have metastatic disease, the usefulness
cancer;247 however, when given to patients who are near of current staging systems is more restricted. In advanced
the end of life, even to those with a relatively good disease, traditional prognostic factors (eg, site of primary
performance status, chemotherapy seldom has benefits, cancer, and number and sites of metastases) might be
and might adversely affect the quality of death.248 Early less relevant because many patients with advanced cancer
involvement of palliative care services can reduce the follow a common disease trajectory of increasing debility,
frequency of chemotherapy administration close to anorexia, cachexia, fatigue, and decreased mobility. This
death, without any adverse consequences for trajectory, in many cases, ultimately leads to confusion,
survival.3,249 In 2008, the UK National Confidential drowsiness, coma, and death.259 In these circumstances,
Enquiry into Patient Outcome and Death250 reviewed simply knowing that a patient has stage IV disease does
deaths occurring within 30 days of systemic anticancer not help to distinguish between patients with prognoses
chemotherapy treatment (SACT). External review of days, weeks, months, or years. Clinicians frequently
suggested that the decision to give palliative SACT was rely on their own clinical judgment or intuition to arrive
inappropriate in 19% of cases (because of factors such as at prognostic estimates. However, systematic reviews
poor performance status, lack of realistic prospect of consistently show that such estimates are often inaccurate
benefit, or end-stage disease). In 27% of patients and overly optimistic.260,261
receiving palliative chemotherapy, external advisers The most commonly used qualitative method for the
considered that the treatment might actually have caused prediction of survival in patients with advanced disease is
or hastened the patient’s death. The authors the so-called surprise question. The surprise question
recommended that, before administering SACT, (“Would you be surprised if this patient died within the
oncologists should fully discuss the aims and likely next X months?”), used either alone or as part of the Gold
outcomes of treatment with patients, including a Standard Framework proactive identification guidance
discussion of the option of no treatment. Moreover, for tool,262 has been recommended as a way to identify
patients with an ECOG performance status of 3 or 4, the patients who might benefit from referral to specialist
authors recommended that palliative chemotherapy palliative care services. A 2017 systematic review263
should only be embarked on with caution and after reported that, overall, the surprise question was accurate
consideration by a multidisciplinary team. on 74·8% of occasions. Although the positive predictive
Discordance between patients’ and clinicians’ per value of the surprise question was low (30%), it performed
ceptions about the intended purpose of chemotherapy is better at screening out those patients who were not

expected to die within a specified timeframe (negative evaluated in 18 studies (n=21 082) in numerous countries
predictive value 90%). and multiple tumour types. In these studies, the PPS can
In response to the inaccuracy of clinicians’ predictions, distinguish between patients with differing survival
an increasing number of prognostic tools have been outcomes.279,280 Prognostic accuracy has not been directly
developed specifically for use in patients with advanced compared with clinician predictions of survival. The
cancer.242,264–266 There is no consensus about the most Palliative Prognostic Index (PPI)271 is calculated using five
accurate or practical tool for clinical use; however, a few clinical variables. The model stratifies patients into three
of the better validated tools are shown in table 3, and are groups: survival of less than 3 weeks, less than 6 weeks, or
discussed below. more than 6 weeks. PPI has been validated in several
The Palliative Prognostic (PaP) score267,268 consists of studies,281,282 and it has the advantage of relying neither on
six variables. Partial scores are allocated to each variable the clinician prediction of survival nor on laboratory
and the total score determines whether the patient is at measures (which can be challenging to obtain in palliative
high, intermediate, or low risk of death within 30 days. care patients). Prognostic accuracy improves if used
The PaP score has been externally validated in several between 3 and 5 days after admission to a palliative care
studies,265 and the original performance of the tool has unit, rather than on admission.283 It is more accurate than
been broadly replicated. The total PaP score is more clinician predictions of 30-day survival, but not 100-day
accurate than a simple clinician prediction of survival and, survival.284 Perhaps the simplest measure is the modified
somewhat paradoxically, its accuracy might be improved Glasgow Prognostic Score (mGPS),272–274 which is
by removing the clinician prediction of survival from the calculated from the amount of serum C-reactive protein
scoring algorithm.277 A modified version of the PaP score and albumin. The mGPS is used to distinguish patients
(including delirium as an additional prognostic factor), with good, intermediate, and poor prognoses.265,285 The
the D-PAP, has also been developed,269 and is more scale is simple to calculate, and has been widely used in
accurate than the original. One criticism of both the PaP various cancer types. Its prognostic value is based on its
and D-PaP scores is that they are heavily reliant on a association with the severity of the cachexia syndrome.286
clinician prediction of survival to generate the overall Feliu and colleagues275 developed a prognostic nomogram
score. The Palliative Performance Scale (PPS)270 was consisting of five variables (ECOG performance status,
developed as a modification of the Karnofsky Performance serum albumin, lactate dehydrogenase, lymphocyte
Status,278 with a focus on patients with poorer mobility or counts, and time from initial diagnosis to diagnosis of
self-care abilities, or both, and the inclusion of other terminal disease) to predict survival at 15, 30, and 60 days.
potentially relevant prognostic indicators. A 2017 In 2011, Gwilliam and colleagues276 reported the
systematic review265 reported that the scale had been development of the Prognosis in Palliative care Predictor
Variables included in score Type of prognostic estimate

Palliative Dyspnoea; anorexia; Karnofsky performance status; total white cell Scores divide patients into three risk groups: (A) >70% probability
Prognostic Score count; lymphocyte percentage and clinician prediction of survival of surviving 30 days; (B) 30–70% probability of surviving 30 days;
(PaP)267,268 and (C) <30% probability of surviving 30 days
Delirium PaP Delirium; dyspnoea; anorexia; Karnofsky performance status; total white Scores divide patients into three risk groups: (A) >70% probability
(D-PaP)269 cell count; lymphocyte percentage; and clinician prediction of survival of surviving 30 days; (B) 30–70% probability of surviving 30 days;
and (C) <30% probability of surviving 30 days
Palliative Ambulation; physical activity and extent of disease; self-care abilities; Patients can be divided into risk groups according to PPS score
Performance oral intake; conscious level of 10−100%; life tables can be used to predict probability of
Scale (PPS)270 surviving to defined time periods
Palliative PPS score; oral intake; dyspnoea; oedema and delirium Patients are stratified into three groups: survival shorter than
Prognostic Index 3 weeks; shorter than 6 weeks; or >6 weeks
(PPI)271
Modified Glasgow Serum C-reactive protein and albumin Patients are stratified into three groups: good, intermediate,
Prognostic Score and poor prognosis
(mGPS)272–274
Feliu Prognostic Eastern Cooperative Oncology Group performance status; serum Using the nomogram a probabilistic estimate can be calculated
Nomogram albumin; lactate dehydrogenase; lymphocyte count and time from for survival at 15, 30, and 60 days
(FPN)275 initial diagnosis to diagnosis of terminal disease
Prognosis in Performance status; anorexia; dyspnoea; global health; breast cancer; Categorical survival prediction: days, <14 days; weeks,
palliative care male genital organ cancer; distant metastases; bone metastases; liver 14–56 days; months+, >56 days
scale A (PiPS-A)276 metastases; mental test score; heart rate; dysphagia; and weight loss
Prognosis in Performance status; anorexia; global health; male genital organ cancer; Categorical survival prediction: days, <14 days; weeks,
palliative care distant metastases; bone metastases; mental test score; heart rate; fatigue; 14–56 days; months+, >56 days
scale B (PiPS-B)276 lymphocyte count; white cell count; neutrophil count; c-reactive protein;
albumin; platelets; urea; alanine transaminase; and alkaline phosphatase
Table 3: Summary of characteristics of palliative prognostic tools

models (PiPS). Two scales, PiPS-A and PiPS-B, have been Communication of prognosis
created so that a prognostic score can be calculated For prognostic tools to provide benefits for patients, the
regardless of whether or not blood test results are clinician must communicate the estimates produced
available. Both scores have subsequently been validated by (including the associated uncertainty) and the impli
external groups.287,288 The PiPS scales produce a categorical cations for treatment clearly and with empathy, so that
output such that patients are stratified according to the information is understood and can be used by the
whether they are likely to live for days, weeks, or months patients. Proper prognostic evaluation and sharing the
(or longer). results with the patient are core clinical skills in
Only a few studies have directly compared the integrated oncology–palliative care. Communication of
performance of the different prognostic tools, and no prognostic information is one of the fundamental tasks
clear pattern emerges. The PiPS tools have been directly in the provision of patient-centred care. For a broader
evaluated against clinician predictions of survival. presentation of communication tasks see the section of
Gwilliam and colleagues276 reported that the PiPS-B tool this Commission on patient-centredness.
was significantly more accurate than a doctor or nurse’s Clinicians have a duty to fully inform patients about
estimate of survival, but was not statistically significantly treatment intent and its risks and benefits; this
more accurate than a combined multidisciplinary team communication is particularly important for SACT
estimate. The PiPS-A and PiPS-B were also reported to because patients often have unrealistic expectations about
be better at predicting short-term prognoses than the its potential benefits.250,251 Although most patients are told
PaP, D-PaP, or PPI, but not as good as the D-PaP at that their cancer is incurable, physicians have a tendency
predicting longer-term prognoses.288 The same study to steer the conversation towards treatment, engage in
reported that the PiPS-A and the PPI were the most collusion with patients’ false optimism, and sometimes
feasible tools to use in clinical practice (routine data fail to check that their patients have understood the
available for >90% of patients). The PaP has been shown purpose of SACT.294–297 Studies297,298 have reported that 50%
to perform better than, or as well as, the PPI289,290 or the or fewer patients were offered alternatives to SACT in
PPS,291 but not as well as the Feliu Prognostic consultations, and that clinicians often described palliative
Nomogram.275 Chou and colleagues292 reported that care as doing nothing, rather than discussing its potential
the PPI performed better than the mGPS in patients benefits. The increasing number of lines of chemotherapy
with haematological malignancies under palliative and novel therapies further adds to the uncertainty facing
care. A large (n=1778) prospective comparative study the informing physician. This uncertainty points to the
(ISRCTN13688211) comparing the accuracy of the PiPS-A need to adhere to one of the basic principles of
and PiPS-B tools with the PaP, PPS, Feliu Prognostic prognostication: it is not an event, but a process.299
Nomogram, PPI, and Glasgow prognostic score, is Furthermore, the patients’ and relatives’ wishes for
currently underway in the UK and is due to report in prognostic information will vary over time.244 The patients’
2019. Importantly, this study also includes several wishes for exact information decreases as death
clinician predictions of survival (probabilistic and approaches but is, in general, ambivalent.244 Involving
temporal) to act as comparators. patients in a continuous discussion of their prognosis
Although accuracy is an important factor when the might influence their future goal setting, enabling them
relative merits of different prognostic tools are compared, to set a goal other than survival.
other factors should also be taken into consideration. There are a range of patient, physician, and institutional
Steyerberg and colleagues293 emphasised the importance barriers to clear communication about prognosis and
of studies assessing the effect of prognostic tools on palliative care in oncology. Oncologists describe a cure
clinical practice and outcomes. The best method for such culture in which they are trained to treat, and so can feel
studies is a cluster randomised controlled trial, but none that stopping SACT is a sign of failure, often resulting in
have been done in the context of palliative care. Impact discussions about hospice being delayed until all treat
studies are required to determine whether more accurate ment options have been exhausted.300 Physicians report
prognostication would lead to earlier referral to palliative little confidence in this communication, particularly
care services, more advance care plans being prepared, related to uncertainty about prognosis, leading to concerns
more home deaths, less intensive treatment in the last that an inaccurate prediction could reduce patient trust.301
weeks of life, and greater satisfaction with communication They also express concerns that breaking bad news could
and with care. lead to depression and a loss of hope in patients.302
In conclusion, the current state of knowledge is Despite these perceived barriers, clear communication
insufficient to make a definitive recommendation about about prognosis early in the disease trajectory must be
the best prognostic tool to use. Nonetheless, there is the aim within oncology. By contrast with the concerns of
good evidence that clinicians’ estimates alone are many physicians, it is possible for patients to maintain
inaccurate and are, generally, overly optimistic. These hope following the disclosure of a poor prognosis.303
estimates should be complemented by the use of Mack and Smith304 argue that this is a common miscon
objective prognostic tools wherever possible. ception, and point to evidence that honest discussions,

even when the news is bad, contribute to better Barriers and solutions
physician–patient relationships that foster hope. A Accurate prognostic information is needed by both
narrative review305 found that avoidance of prognostic patients and clinicians to help inform treatment decisions.
discussions can lead to mistrust, anxiety, reduced quality Clinicians’ survival predictions are frequently inaccurate
of life, and family distress. and overly optimistic. Professionals working in oncology
Given the focus on quality of life in palliative care, often do not have confidence in communicating poor
satisfaction with communication is, perhaps unsur prognoses and related uncertainty, resulting in these
prisingly, higher for bereaved relatives in hospice conversations being delayed or omitted, and in patients
settings than hospitals.306 Therefore, earlier integration having unrealistic treatment expectations. Some of these
of palliative care specialists might increase patient barriers could be overcome by the use of objective
prognostic aware ness, and improve patient and prognostic tools to complement clinical intuition; however,
caregiver satisfaction. In randomised trials integrating further research will be required before definitive
palliative care from the time of diagnosis, including recommendations can be made. Earlier integration and
regular appointments with a palliative care specialist, increased collaboration between oncology and palliative
Temel and colleagues3,50,307 found that early palliative care care might improve the quality of communication and
interventions improved quality of life, prognostic reduce the frequency of futile treatments in patients
awareness, and communication about end-of-life approaching the ends of their lives. Evidence-based
preferences. communication guidance and training (as part of a wider
In addition to the involvement of palliative care integration of palliative care and oncology education; see
specialists early in the disease trajectory, oncologists the section of this Commission on the role of education) to
need practical advice on communication strategies to provide practical strategies for the communication of
integrate early and honest discussions about prognosis prognosis and uncertainty would reduce barriers to
and palliative care into their own practice as part of an prognostic awareness among patients (panel 6)
SCP. Some guidance on strategies that can be used
during conversations about prognosis and other end-of-
life issues is given in panel 5.
Panel 5: Australian clinical practice guidelines for
In a review and synthesis of best practices, Bernacki
communication of prognosis and end-of-life issues
and Block305 suggest the use of a conversation guide to
ensure key topics, such as goals, fears, and trade-offs • Assess what the patient already knows and the level of
(ie, prolonging life through intensive treatment vs detail they want
quality of life) are covered. Several discussions might be • Tailor the information to the individual and their family:
needed to allow for a step-wise approach that develops pace provision of the information depending on the
prognostic awareness,309 and to adapt infor mation individual, use non-technical language, consider the
provision as the disease progresses and the patient’s family’s individual needs
communication preferences change.26,310 Raising these • Acknowledge uncertainty and avoid giving exact
issues early in the disease trajectory allows the time timeframes; be honest without being blunt
needed for such a step-wise approach. From the patient’s • Explore and acknowledge emotions
perspective, adjusting their hopes and expectations for • Encourage questions, check understanding, and emphasise
the future—from where they are to the factual continuing care
situation—is, for most, a process that takes time. The
Panel adapted from Clayton and colleagues.308
conversation guide suggested by Bernacki and Block305
might be particularly useful as a starting point for
clinicians with little experience of prognostic
conversations. For clinicians who will be having regular Panel 6: Prognostication—recommendations
prognostic discussions, more focused communication • Prognostic communication about life expectancy should
training about cultivating prognostic awareness might occur early in the disease trajectory as a part of early
be appropriate. integration of palliative care, which can be achieved by
Systematic reviews of training to improve clinicians’ teaching oncologists and palliative care physicians how to
end-of-life communication and communication with convey prognostic information, and establishing national
patients with cancer have reported some positive results, and international indicators of patient involvement in the
such as increasing expressions of empathy, increased use prognostic process
of open ended questions, and improved clinicians’ • Develop new prognostic tools to predict survival,
self-efficacy and comfort with these conversations.311,312 symptom control, and maintenance of functions
However, more evidence is needed about the effect of (physical, mental, and social) during cancer palliative care
training on patient satisfaction, whether positive effects by allocating research resources and establish international
are sustained over time and on other outcomes, such as collaboratives to develop the prognostic tools
quality of patient death.311,312

Patient-centredness—content, method, and substantial. Evidence exists that oncologists might have
clinical implications significant deficits or shortcomings in their emotional
The Institute of Medicine defines patient-centredness as, engagement and communicative skills with their
“care that is respectful of, and responsive to, individual patients,321 and that both empathy and communication
patient preferences, needs and values, and ensuring skills can be improved with training.320,322
that patient values guide all clinical decisions”.313 This Patient-centredness has been central to contemporary
approach is recommended in all areas of medicine, but its palliative care since its emergence in the 1960s. At that
content and methods have been considered particularly time, patients did not receive palliative care until near the
appropriate in cancer care.314 Central to this approach is end of life, when it was clear that symptoms, needs,
patient-centred communication that aims to foster healing concerns, and relationships would be the primary targets
relationships, exchange information, respond to emotions, for interventions. Palliative care is now recognised as
manage uncertainty, make decisions, and enable self- potentially of value from the time of diagnosis, but the
management.315 Patient-centred care is dynamic and focus on patients and families has remained central to
should involve a step-wise approach addressing the palliative care. Quality of life and symptom alleviation
patients’ physical, psychological, social, and spiritual are primary targets of treatment in palliative care, and
needs at all stages of the disease.313 These needs must be communication and SDM are considered essential
assessed and documented dynamically because they are methods of practice.
likely to change over time and will be used in the decision- SDM has been defined as an approach where clinicians
making process in consultations, multidisciplinary team and patients share the best available evidence when faced
meetings, or other clinical decision points. with the task of making decisions, and where patients are
Increasing research attention is being paid to value- supported to consider options, to achieve informed
based care in cancer, which refers to the quality of care preferences.323 SDM involves both the patient and the
achieved, modified by the cost.316 Up until the past two physician, and helps to ensure that there is informed
decades, patient-reported outcomes were not included in consent and patient autonomy in decision making. SDM
the research evaluation of the quality of cancer care, and presupposes that the patient has knowledge of the
unfortunately the clinical focus still tends to be disease disease, intended effects and toxicity of treatments,
centred, rather than patient centred. This focus has expected survival, and symptom burden with and without
contributed, at least in high-income countries, to the the proposed treatment. SDM requires a trusting
overuse of some cancer treatments, including those that relationship between the patient and the health-care
are futile, and to the rising cost of cancer care.317 The use providers, and communication skills on the part of the
of PROMs in clinical trials and some clinical practices health-care providers. Such skills are needed to facilitate
has facilitated the shift to greater patient-centredness in the appropriate, timely, and sensitive sharing of relevant
cancer care. information, and to support patients in expressing their
Systematic symptom assessment is an important preferences and views, and in making truly informed
component of patient-centred care. Studies75,76 done in choices.324
the past few years have shown the positive effects of Advance care planning (ACP), a particular variant of
systematic symptom assessment on patients’ quality of SDM, focuses on the patient’s priorities for the future,
life, and possibly also survival. However, despite the including dying in accordance with their personal values
overwhelming evidence of the benefits of systematic and wishes. ACP is an important aspect of contemporary
symptom assessment, implementing such assessments cancer palliative care,324 recommended to take place early
in routine cancer care has been slow because of concerns in the course of treatment when cure is not an option.
about its feasibility, benefit, cost, and the absence of a Engagement of patients and families in ACP can help
strong enough system of implementation with economic them to reflect on, and manage, the transitions that lie
or professional incentives, or both, and a patient-centred ahead, and to set treatment goals that are consistent with
focus.72,76,126,318,319 their values and preferences.325
Adequate communication skills are necessary to provide The integration of palliative care and oncology highlights
patient-centred care. Patient-centred communication can the importance of patient-centredness, including skills in
be learned,320 and must be regarded as a professional skill, communication, SDM, and ACP. Although responsibilities
rather than merely a personal attribute. This competence of oncologists and specialists in palliative and supportive
is needed to assess symptoms, provide information about care should be divided to some extent, communication
diagnosis and disease progression, and to discuss options and interaction between them is important to support a
and patients’ preferences for treatment and care.315 Such common understanding of the disease and the treatment.
skills are of importance throughout the entire cancer Feeding back palliative medicine specialists’ observations
trajectory, but might be particularly relevant when the to oncologists might help to ensure that patients are truly
treatment intention is non-curative, or the biological informed and do not have unrealistic expectations about
effects of tumour-directed treatments might be minimal the goals and results of the tumour-directed treatment,
and the adverse effects on quality of life might be ensuring they can meaningfully participate in SDM.326

Patient-centredness in palliative care and oncology

settings Panel 7: Main elements of patient-centred care
Cicely Saunders established modern palliative care,
31
• Respect for patients’ values, preferences, and expressed
highlighting the importance of active listening to needs
patients’ needs, and making patients’ views visible and • Coordination and integration of care
recognisable in the care processes. She also introduced • Information, communication, and education
the concept of total pain,327,328 which infers a broad • Physical comfort—relief of bothersome symptoms
understanding of the patient’s needs during a life- • Emotional support—relief of fear and anxiety
limiting disease. Saunders was a pioneer in patient- • Involvement of family and friends
centred care, although this term had not yet entered the
medical lexicon at the time.
Some characteristics of contemporary cancer care are nature of the cancer care system, with multiple levels of
of relevance to the promotion of patient-centredness as a care, providers, and locations, also presents major
means to improve care. Most patients experience cancer challenges to coordinated care and the development of
as a chronic disease, although the public perception of comprehensive treatment plans.333
cancer is probably more closely aligned with the acute
disease model.329 The chronicity of cancer stems from the Shared decision-making (SDM)
fact that many patients either undergo life-prolonging SDM is a central component of patient-centred care and is
treatments for years, or are cancer survivors with highly relevant in all phases of cancer treatment, but
manifest or latent distressing symptoms and signs. The becomes increasingly important as the disease progresses.
chronic disease model has become even more relevant to Decisions often become more complex with disease
cancer over the past few decades, with the advancement progression, with trade-offs between life quantity and life
of modern surgery, chemotherapy, radiotherapy, targeted quality. SDM is an active process, requiring the exchange
therapies, and various types of immune therapies. of information and opinions for patients to make decisions
Cancer treatments are often combinations of different on the basis of their values and preferences, and their
treatment modalities administered by different understanding of the best available medical evidence.334
specialists, and each treatment carries its own risks and This means combining the tumour-directed and patient-
benefits. Navigation of such complex systems therefore centred approaches to care, and weighing the benefits and
becomes a core task in itself, which the patient cannot be risks of starting, changing, continuing, or stopping
expected to solve alone. tumour-directed treatment. Decisions about selecting one
To be actively involved in the care planning, the patient, treatment option over another might also be difficult
and eventually their family, must understand and accept because there is often little or no empirical data that
the reality of the situation, and the options at hand. indicate greater value for one regimen over another.335,336
Many patients’ understanding of their disease is far from Various factors unrelated to the value of care might
their medical reality. Combined with the distress that affect SDM, including those highlighted by researchers in
accompanies the cancer disease trajectory,330 the physicians behavioural economics and the psychology of decision
meet patients who are often misinformed or under making.337 Decisions about starting, continuing, or
informed, and have compromised decision capabi lities discontinuing chemotherapy or other cancer treatment
due to distress. These patients are, therefore, at high risk might be difficult to make because of insufficient,
of accepting treatment proposals with uncertainties that uncertain, or even conflicting empirical data, and because
they are not aware of. This situation places a great they are made under circumstances of emotional strain.
responsibility on the physicians because they might begin In this situation, available statistical and clinical data
treatment of patients who are not truly informed about the might not be used,338 and some clinicians might find it
risks and benefits of the treatment. The high percentages easier to prescribe another round of chemotherapy than to
of patients misinterpreting palliative radio therapy or engage in a conversation about futile treatment.337 The
chemotherapy as curative support this understanding.331 last-case bias might operate in situations in which decision
Patient-centred care is a broad approach that must take makers are more influenced by recent experiences than by
into account both the person and the disease, with remote events. Reimbursement practices might also
attention to individual values, needs, resources, and directly or indirectly influence institutions and providers
preferences (panel 7). Health literacy332 (ie, the ability to toward chemotherapy that is costly, but of uncertain
obtain, read, understand, and use health-care infor benefit. Patients and providers might tend to be treatment
mation) might vary widely across patients, and must be focused in such situations of uncertainty339 because they
taken into account in communication and SDM. Various hope that treatment will prolong survival, or because
factors, including anxiety related to the life-threatening physicians are uncomfortable having conversations
circumstance, language, culture, and recent immigration, regarding prognosis.339 Correction of misbeliefs about
might affect health literacy and the ability of patients to quantity of life and introduction of alternative treatment
participate in decisions about their care. The fragmented goals, such as preserving quality of life, require

of life is both extensive and expensive,24,257 although such

Physician’s premises Patient’s premises
treatments often reduce quality of life and time spent at
Physician makes the decision Physician makes the decision without Patient is not competent to give home.251 Paradoxically, physicians who develop cancer
access to patient’s preferences informed consent
tend to choose less intensive treatment for themselves at
Physician limits the patient’s Physician clarifies available Patient wants a treatment that
preferences treatment options is not available end of life than they offer their patients.345
Physician makes decision in Physician recommends a defined Preferences and wishes for shared A common misunderstanding is that SDM involves
collaboration with the patient treatment decision-making might vary leaving decisions to the patient. As shown in table 4,
Patient makes the decision during Physician presents equivalent or Preferences and wishes for shared there are different degrees of SDM, which depend, in
the consultation with their physician similar treatment alternatives decision-making might vary part, on the choices at stake. The decision-making
process is the main component of SDM.
Table 4: Examples of different degrees of shared decision-making
To promote SDM, the doctor must encourage patients
and caregivers to participate in consultations and
decisions regarding the care, determine situations in
Action Consideration
which this is crucial, and inform patients about the
1 Determine situations in which shared decision- Complexity depends on treatment intent and options benefits and disadvantages of available treatment
making is crucial
options. This process must include balanced prognostic
2 Acknowledge that decisions are to be made to Increasingly important with sensitive issues
the patient
information about best-case and worst-case scenarios,
3 Describe treatment options, including risks, Avoid hastened decisions, make sure patients are
responding to patients’ concerns and their understanding
benefits and uncertainty associated with options fully informed of the information, which helps to reach an agreed-on
4 Elicit patient preferences and values, and make Listen carefully and convey information in a language treatment plan.346 This approach largely corresponds
sure the patient understands the information in that matches the patient’s cognitive level with the five-step process presented in table 5. Patients’
her or his perspective and caregivers’ assertive behaviours and physicians’
5 Agree on a plan for the next steps in the Agree that the plan might be revised depending on facilitative behaviours interact to promote patient
decision-making process the disease development
participation in the decision-making process over time.347
Table adapted from Politi and colleagues.334 This complexity explains why a single, unidimensional
intervention is less likely to work.348
Table 5: Five steps in shared decision-making
The literature on outcomes of SDM in palliative care is
scarce and findings are inconclusive.349 However, in a
communication skills on the part of the physician, and are range of studies in different groups, SDM has been
most appropriate within the framework of SDM. associated with better quality of life and treatment and
Physicians are legally and ethically obligated to provide consultation satisfaction, better affective-cognitive out
information in a way that enables patients to be active comes, and decisions that are more in line with the
and informed partners in the decision-making process patient’s preconsultation treatment preference. A 2017
and to promote their participation in decision making.340 study350 showed that 50 (49%) of 102 patients with cancer
A process to accomplish such SDM can be described in preferred shared responsibility of treatment decisions,
four steps: awareness of equipoise, discussion of the whereas 30 (29%) patients preferred to leave the decision
benefits and harms of options and their probabilities, to the physician. Older and more distressed patients
elicitation of patients’ concerns and expectations, and were more likely to leave the decision to the physician.
partnership and participation.341 Only the second step This corresponds to another study351 reporting that about
seems to be common in cancer clinics,342 where most 50% of patients with advanced cancer preferred to be
attention is typically paid to the objective biological involved in SDM, whereas the remaining 50% were
aspects, consistent with the tumour-directed approach. almost equally divided between active (ie, making the
Little attention is often paid to the patient’s (ie, host’s) decisions by themselves) and passive (ie, the physician
preferences, symptoms, quality of life and care, and the making the decision for them) approaches. Such attitudes
option of no tumour-directed treatment. might change over time, in either direction, pointing to a
Despite being a central element of patient-centred care, need for individualisation and flexibility in
SDM is not explicitly included as an integrated part of communication and care planning. More research has
oncology guidelines.15,21 A premise of SDM is that the been done on the use of decision aids, finding increased
oncologist and the palliative medicine specialist must knowledge, greater patient engagement, and decisions
both be aware of the patient’s prognosis and of the risks more consistent with patients’ preferences as a result of
and benefits of treatment choices in patients with their use.352
advanced cancer.343,344 Patients might have unrealistically There is little evidence about patient preferences
positive perceptions of their prognosis and effects of concerning communication and information as an aid
tumour-directed treatments, and be willing to continue to SDM in palliative oncology.353 Most patients (90–95%)
or to start therapy with minimal or no likelihood of are more willing to obtain information about diagnosis,
therapeutic effect and a high risk of side-effects.331 The prognosis and treatment options than about palliative
use of intensive and non-beneficial treatment at the end care (63%).354 However, about half wish to participate in

treatment decision making as time passes, and patients personal values, life goals, and preferences regarding
with more pain are more likely to change their future medical care. The goal of ACP is to help to ensure
preference towards being more involved.355 Most that people receive medical care that is consistent with
patients with advanced cancer say they want honest, their values, goals and preferences during serious and
sensitive com munication about end-of life issues.356 chronic illness.”366 The word process underlines that the
This kind of communication helps patients and their planning is not a one-time event, but evolves over time
families to prepare, make informed decisions, and avoid through a series of conversations; therefore, ACP
potentially burdensome medical treatments near documents should be updated regularly.363,365,367 Although
death.357 the definition does not specify who should take part in
The role of family and caregivers is important in the process, ACP discussions commonly involve the
the SDM process throughout the disease trajectory. patient, family, informal caregivers, and health-care
Two-thirds of patients with advanced cancer want family professionals. This discussion can be had by the primary
members to participate in the communication and care or oncology team, or by the palliative care team,
decision making;354 however, caregiver preferences depending on the available skills and resources.
might not be concordant with those of the patient,358,359 The ACP process starts by exploring the patient’s
especially regarding information when death nears.343 health-related experiences, concerns, personal values,
Some patients with cancer might want to spare family and understanding of ACP and readiness to engage in it.
members from the emotional strain of receiving bad Not all patients want such a plan or can formulate their
news, and distress in caregivers of patients with wishes for future care, which is, in itself, valuable
advanced cancer is reported to be greater than in the information for planning of care. The current disease
patients themselves.360 situation should be discussed next, to obtain a common
Successful implementation of SDM in clinical practice understanding of treatment and care options and their
relies on training physicians to engage with the patients advantages and disadvantages. ACP might also include
and provide the right information at the right time. discussion and completion of an advance directive or
Several decision aids exist to facilitate this process,21,334 living will, depending on the national legislation. The
and the step-wise approach presented in table 5 is a advance directive will typically address specific
systematic approach. Specifically defining SDM as a part interventions, such as cardiopulmonary resuscitation or
of the standardised care pathways might promote its tube feeding, in a future scenario of incapacity. Finally,
implementation in clinical practice at the organisational encouraging the individual to share thoughts and
level and the individual patient care level. preferences with family and friends is an important part
of the process.363,365,367
Advance care planning (ACP) Different forms and templates for ACP documents
ACP can be considered a variant of SDM, focusing on the have been proposed, and many are freely available on the
patients’ voluntary participation in discussing their internet.368 Debate about whether ACP should be based
future care with their care providers. ACP should be an on open or scripted conversations is ongoing.324 The use
integral part of the care and communication process, and of a template might ensure that the most relevant areas
of the regular care plan review. ACP differs from regular are presented to the patient, although strict adherence to
care planning by focusing on anticipated deterioration in a guide might restrict the free exchange of thoughts, and
the individual’s condition approaching death. ACP was reduce ACP activity to a tick-box exercise.365 A semi
developed from advance directives, which have been structured interview guide might avoid these dangers.369
used in the USA and other countries since the mid- ACP ensures that the care is more likely to be in
1970s.361 From the mid-1990s, the focus of advance accordance with the patient’s preferences than if it is not
directives shifted from standardised legal forms to an done.370 It has also been shown to decrease life-sustaining
ongoing and flexible process, and from refusal of treatment at the end of life, increase the use of hospice
treatments to promotion of statements of preferences and palliative care, and prevent unwanted hospital
and wishes, paving the way for ACP.361,362 ACP has admissions.357 Comprehensive ACP programmes seem
received growing attention since that time, and is now an to be more effective in making end-of-life care coherent
important issue in palliative care internationally.324,363 In with patients’ preferences than completing a written
Europe, efforts to promote ACP have been focused on advance directive.371
patients with life-limiting illnesses, rather than on the Although unresolved questions as to the optimal ACP
general public.364,365 Although advance directives are system and how to assess the impact and effectiveness of
specifically directed at refusing treatment when the system remain, ACP is coherent with patient-centred
individuals are no longer able to express their wishes, care and therefore relevant for the early integration of
ACP also concerns future care in a broader sense.363,365 palliative care and oncology. Presently, many countries
A consensus definition of ACP, published in 2017, do not have any legislation regarding ACP, which we
describes it as “a process that supports adults at any age think is necessary for successful integration of palliative
or stage of health in understanding and sharing their care and oncology.

Systematic assessment of the patient’s perspective The most feasible and reliable form of PROMs is via
Symptoms, preferences, and patient-reported outcomes standardised and methodologically sound self-report
have had many different labels over the past three to four questionnaires, which are traditionally paper-based. New
decades. The FDA proposed the term PROMs for all advances in health information technology have led to
measures that can best be assessed by patient self- the development of electronic tools for the collection of
report.66 PROMs is an umbrella term covering the PROMs. Electronic data collection permits dynamic
patient’s perspective on wellbeing, symptoms, subjective assessment—ie, automatically tailored questions for
treatment effects, and side-effects.67 The CONSORT-PRO individual patients based on the patient’s previous scores
Extension Statement, which aims to improve the on given symptoms. This dynamic assessment results in
reporting of PROMs on symptoms, functioning, and fewer repetitive and irrelevant questions, reducing
quality of life,69 further consolidates PROMs as patient burden. Several electronic questionnaires, so-
independent outcomes in cancer.68,69 called e-PROMs, now exist, with a user-friendly interface
The patient perspective and experience cannot be and immediate aggregation, storage, and transfer of
replaced by clinical observations and examinations by the patient scores for direct use in the clinical encounter and
oncologist or palliative medicine specialist. In ordinary possible integration with other clinical data in the
consultations, many symptoms are not identified or electronic patient record.386 In the oncological setting,
addressed;372 however, PROMs can be used to highlight electronic assessment and rapid presentation of results
the patient’s experience and bring the patients’ voice into to the clinician facilitate communication, are well-
the clinical consultations. The benefits of routine accepted by patients and clinicians, and might result in
assessment of PROMs in clinical practice are well more efficient and focused use of time.71 A 2012
documented, including improved patient–physician qualitative study73 showed that perceived usefulness
communication,373–375 increased physicians’ awareness of might be more important than functional aspects
patients’ physical and psychosocial functioning,376–378 regarding applicability; however, immediate display of
improved patient wellbeing,75,374 and a more efficient and easily interpretable results to the physician is a crucial
focused use of time.377 Regular use of PROMs makes the factor for successful implementation of electronic
physician aware of symptoms they did not know affected identification of PROMs in the clinics.74 Nevertheless, the
their patients.378 most important obligation on the part of health-care
Knowledge of symptoms is essential information for providers is to actively use PROMs tools, discuss the
the primary cancer diagnosis and for follow-up care scores with the patient, explain potential interventions,
during curative and life-prolonging treatments; however, and make the patient an active partner in the decision-
systematic symptom assessment is not part of routine making process.
oncological care376,379–381—although it is frequently used in Systematic symptom assessment by either paper-based
clinical trials.382 For patients with advanced cancer, for or e-PROMs ensures registration of burdensome
whom symptom management is a central goal of care, symptoms, such as anxiety and depression. This process
systematic use of PROMs is even more important, and is is important because patients often do not report such
a prerequisite for optimal symptom management. symptoms unless asked, particularly if they perceive that
Relieving burdensome symptoms is therefore a core task they will not be regarded as relevant to their cancer care.
within patient-centredness, and a special obligation on The symptoms reported by the patients with PROMs
the part of the physicians. must be addressed in the clinical encounter and used in
Insufficient and unsystematic assessment of symptoms the decision-making processes. Intensity is the most
is a major factor explaining inadequate symptom relief in common dimension that is investigated in the
patients with cancer. Inadequate pain control has been assessment tools, but must be supplemented with other
documented in up to half of patients,383 despite efforts to symptom characteristics. The duration of the symptom,
improve pain treatment.383,384 Clinical studies of patients its meaning, and the distress associated with it might
with cancer have found systematic use of PROMs to best be elucidated in a follow-up clinical interview.
improve a range of symptoms, including pain.377 Initially, this assessment might be done in an oncology
For patients with limited life expectancy, the balance clinic, but a more in-depth assessment might be done by
between treatment effect and tolerance of therapy is the specialised palliative care or psychosocial oncology
crucial in treatment decision making. Reporting of team to be able to provide more specialised care.
toxicities and adverse effects in clinical trials, by such
systems as the Common Terminology Criteria for Adverse Caregiver involvement
Events (CTCAE, version 4.0) developed by the National Patient-centred care and SDM aim to involve the family
Cancer Institute, is mandatory. Until about 7 or 8 years members of patients. In clinical care, patients should be
ago, the CTCAE were rated by physicians, although many routinely asked to identify their significant others, and to
criteria are symptoms that are best reported by the provide information about the nature of their relationship,
patients. This recognition has led to the development of a strengths and limitations in their ability to take on
PROMs version of the CTCAE—the PRO-CTCAE.385 complex cancer caregiving, and how much information

about the medical situation they can and should receive. significantly lower depression scores at 3 months in the
Caregiver problems, such as serious illness or emotional intervention group.
or economic problems, also need to be assessed. Two consecutive meta-analyses388,389 have examined the
Caregivers are often actively involved in decisions about effect of different interventions on various caregiver
the care and treatment of a patient with cancer, particularly outcomes in a total of 79 randomised trials with family
decisions focusing on the end of life. Patients choosing to caregivers of patients with cancer. Results from the first
participate in SDM are reported to prefer to share this analysis389 indicated these interventions had small-to-
experience with their family members.387 Caregivers, medium effects on caregiver burden, ability to cope, self-
including family or friends, often provide care for patients efficacy, and aspects of quality of life. In the period covered
with cancer, although many might not be well prepared to by the second analysis388 (2010–16), the number of trials
do so. The burden of such caregiving might be substantial, had increased substantially, corresponding to a huge
and reduced quality of life, distressing symptoms (eg, variety of formats and types of interventions. This
insomnia, fatigue, anxiety, and depression), and financial variability makes comparisons and conclusions about
stress have been shown to be common among care efficacy difficult, but indicates caregiver interventions can
givers.388,389 The strain on caregivers might have increased vary and probably should be flexible.388 In most randomised
in the past 20 years, because cancer care has shifted trials of early introduction of palliative care, caregiver
towards outpatient and home-based care. Moreover, with satisfaction is, at best, defined as a secondary outcome,
cancer being more prevalent in the elderly, many caregivers and therefore can be interpreted as a complementary
are of advanced age and might suffer from substantial effect of improved patient care, and not the result of
health problems of their own. Involvement, training, and specific interventions directed at the caregivers.
support of caregivers are, therefore, key components of Qualitative data from trials of early palliative care have
modern cancer care. identified certain aspects of palliative care that might
Caregiver resources, the quality of the support for the influence the caregiver satisfaction; eg, building rapport,
patient, and the quality of the caregiver support might establishing a relationship with patients and family,
have a decisive influence when the disease progresses focusing coping, and providing realistic information
and decisions need to be made about the place of care about prognosis.326,396 The content of the early and
and the location of death.390 Family members, as informal subsequent palliative care visits, identification of key
caregivers, are often the patient’s main source of issues, and timing of when to address these were
emotional and practical support, although the burden regarded as reasons for favourable outcomes in one
and challenges of disease might create or intensify family study.326 Statements expressed in another study396 gave
conflict. Such conflict, which can obstruct or complicate important clues as to how incurable cancer affects the
treatment planning, might benefit from intervention; family and ways that helped them cope. Statements like,
however, these disagreements can be challenging and “It is the family that’s going through it”, and “Talking
time-consuming to resolve. Palliative care physicians and with the palliative care physician was immensely
teams can help to support caregivers in addressing these advantageous”, clearly illustrate these points.
conflicts, though engagement of specialised psychosocial
oncology might also be of value. The updated ASCO Communication—a key to patient-centredness
Clinical Practice Guideline15 on integration of palliative Oncologists and palliative care specialists face difficult
care and oncology emphasises that services by communication situations throughout the trajectory
multidisciplinary palliative care teams complement of cancer, including breaking news about disease
existing programmes, and “Providers may refer family progression and non-response to tumour-directed
and friend caregivers of patients with early or advanced treatments. A strong focus on better communication as
cancer to palliative care services.” part of early palliative care promotes patient-centred care,
Studies of the effects of early provision of palliative care and results in improved prognostic awareness and
on caregiver satisfaction with care, quality of life, and patient satisfaction.5,307
emotional distress have produced conflicting results. A Patient-centred communication is a key asset for
Norwegian study391 showed an overall positive effect on the implementation of SDM in oncology practice. As
quality of life, in line with studies of caregivers of patients mentioned earlier, the main characteristics of patient-
with a poor prognosis treated by specialty trained centred communication are attention to the patient’s
palliative care clinicians.392–394 The ENABLE III study by affective states, values, needs, and preferences.340 Patient-
Dionne-Odom and colleagues395 was probably the first centred communication aims to create a dialogue
randomised trial to examine a specific palliative care between the physician and the patient; therefore, the
intervention for family caregivers of patients with clinician must be able to monitor and consciously adapt
advanced cancer. The intervention group received three the communication to meet the patient’s needs. When
structured telephone coaching sessions each week and this does not occur, the communication takes the form of
monthly follow-up and bereavement calls, whereas the a monologue that is provider-centred and not patient-
control group received usual care. The results showed centred.

life.398 Honesty is commonly believed to undermine

Panel 8: Communication in the cancer care setting hope, although there is evidence that honest but
Communication will help patients to: empathic communication might actually help to
• Receive bad news preserve morale and psychological wellbeing.230 Finally,
• Handle the emotional impact of a life-threatening illness both parties need to share knowledge and
• Understand and remember complex information understanding, and must have suitable perceptual and
• Communicate with multiple health professionals linguistic skills to produce effective communication
• Understand statistics related to prognosis behaviours that are appropriate to the situation.
• Deal with uncertainty while maintaining hope For patients, good communication with their
• Build trust that will sustain long-term clinical relationships physicians can help to make them feel understood,
• Make decisions about treatment, possibly including participate actively in the interaction, improve their
participation in clinical trials understanding of the disease and treatment options,
• Adopt health-promoting behaviour cope better, and trust in their physicians and the health-
care system. Patient-centred communication can also
Panel adapted from Epstein and Street.315
result in a treatment plan that is concordant with the
patient’s preferences and values. The establishment of a
common understanding of the current situation between
Panel 9: Advanced cancer the patient and physician is essential as the starting point
Key communicative tasks to be solved for patient involvement. Prerequisites to good com
• Elicit the patient’s report of symptoms munication are the use of a mode of delivery and
• Communicate prognosis while maintaining hope language that match the patient’s cognitive and
• Make decisions about tumour-directed and intensive intellectual abilities, and the consideration of the
medical treatments—particularly about starting and patient’s emotional state at the time of the consultation.
stopping criteria Hence, provision of sufficient information requires
• Make decisions about future care, including hospice care knowledge about how to convey the information in an
• Respond to the emotions of the patient, family, and understandable manner at the right time.
caregivers With more complex clinical conditions and therapeutic
• Help the patient navigate the transition to end-of-life care opportunities, patient-centred communication is es
pecially salient.399,400 Nevertheless, although listed as a
key dimension of patient-centred communication,
The key tasks to be solved by patient-centred communi inadequate communication about prognosis and treat
cation span the whole cancer trajectory, but common ment choices is common.343,344,401 Crucial information
features to all phases are exchanging information, about prognosis and treatment options is often not
responding to emotions, fostering healing relationships, discussed during life-prolonging treatment, and might
managing uncertainty, making decisions, and enabling lead to unrealistic patient expectations regarding
patient self-management (panel 8).346 Patient-centred cure.3,307,346 Much too often, these discussions take place
communication transcends medical issues and also late in the disease trajectory, often in the last month,
includes practical issues, such as clarification of which is too late for patient and family to benefit from
responsibilities and who to contact.305 Key communicative referral to palliative care.402
tasks to be solved in advanced cancer are presented in The tendency of physicians to avoid honest
panel 9. communication is not supported by empirical research.
Communication includes both the sending and Parker and colleagues343 found that up to 90% of patients
receiving of information, with both verbal and non- with advanced cancer want information about the
verbal elements. Both parties must repeatedly change disease, treatment options, symptom management, and
roles from sender to receiver; being the receiver life expectancy. Evidence that early discussions about
(ie, performing active listening) is challenging for care goals in advanced disease improve end-of-life
many physicians. One of the most cited studies397 of outcomes is accumulating.305 Patients who have discussed
physicians’ communication showed that general the future with their doctor before the disease is too far
practitioners interrupted the patient, on average, advanced report greater wellbeing and have fewer
18 seconds after the patient had started talking. unwanted intensive interventions in the last weeks of
Physicians must be willing to see patients as whole life, with no detrimental effect on survival.3,357 Earlier
people and provide them with information that is integration of oncology and palliative care with patient-
understandable and useful from their perspective. centred communication enhances patient and family
Physicians must also be prepared to discuss the end of involvement, guides decision making, and promotes
life, although the words die and death are generally realistic expectations for the future. Therefore, patient-
avoided by oncologists, who might be uncomfortable centred communication is important for the im
engaging in meaningful discussions about the end of provement of general oncology care.396

Communication skills can be taught to medical protocols and guidelines. This contrasts with findings414
undergraduates and postgraduates, but discussion of that depression is the main factor associated with poor
prognosis and at relevant timepoints must also be part of quality of life in patients with advanced cancer.
oncology and palliative care training. Such discussions Symptoms of depression,330 demoralisation,415 and
presuppose detailed knowledge about prognosis, spiritual distress416 are common in patients with advanced
including the uncertainty inherent in a prognostic cancer, and longitudinal research417 has shown that, with
evaluation. Empathic communication about prognosis out intervention, these symptoms tend to worsen with
and uncertainty are communicative skills that should be greater proximity to death. Evidence of the effectiveness
mandatory in the curriculum for oncologists and other of psychological interventions to alleviate depression
clinical specialties treating patients with cancer (see the and other manifestations of distress in patients with
sections of this Commission on prognostication and the advanced disease is growing. These interventions include
role of education). supportive-expressive group therapy,418 meaning-centred
As outlined in the scheme for SDM, treatment options psychotherapy,419 problem-solving therapy and behavioural
should be explained simply and clearly. Most topics are activation,420 and dignity therapy.421 However, at present,
emotionally loaded for the patients and their family psychosocial interventions and skills are not well
members. Learning how to elicit and respond to integrated into either oncology or palliative care.
emotions during the consultation while still carrying it An approach to psychological care of the patient with
forward is a skill that physicians must acquire. Very few advanced disease that is integrated with both cancer care
physicians learn these skills by themselves: some and palliative care is the Managing Cancer and Living
improve through engagement in an open professional Meaningfully (CALM) approach, developed in 2014.422
culture focusing on treatment of the patients, and most This intervention is intended to provide patients and
probably need specific training. their caregivers with reflective space to communicate
Training in SDM as a method in clinical practice and their experience, and to address the major decisions,
on how to maintain, develop, and share fundamental burdens, and adaptive challenges of advanced and
communication skills, is needed at regular intervals for progressive disease. Palliative care, oncology, and
oncologists, palliative care specialists, and other health- psychosocial care providers can be trained to deliver this
care providers to foster patient-centred communi intervention, and such training has the potential to
cation.326,403 Empathic listening, flexible and attuned enhance their ability to engage empathically in sensitive
responsiveness to the shifting needs of the individual conversations and to create reflective space. An inter
patient, and to patients’ and caregivers’ emotions are national training programme for health-care providers is
important skills that can be improved;305,309,396,404,405 however, now underway423 for this intervention, which has been
the best methods for improving communication skills shown to alleviate and prevent depressive symptoms,
are not yet established.406 Interventions such as com reduce death-related distress, and enhance the capacity
munication skills training with role play and feedback, of patients to communicate with their family and health-
e-learning, group discussions, modelling, case evalu care providers.424 This programme provides training of
ations, and coaching are some of the most commonly members of the multidisciplinary palliative team. The
used strategies. Strategies that involve activity and palliative care multidisciplinary team is set up to address
practice are most efficient.406 Although less common, the complexity of problems facing the patients and their
interventions that aim to influence the patient’s families. Patients’ problems are often complex and
behaviour, including encouraging them to use prompt cannot be solved by a single profession alone. Some
lists, can be combined with patient and oncologist problems are best addressed by specific members of the
coaching.407,408 Although evidence about their usefulness team—eg, financial problems often need the competence
in palliative care patients is scarce, these interventions of a social worker. The effects of a multidisciplinary
could help to engage patients and physicians in more approach have been shown425 but perhaps not yet fully
active and deep interaction.334,409,410 used. Although a broader patient-centred approach on
the part of the physician seems pertinent, other members
Psychosocial care of the team are often in better positions to provide the
The prevention and alleviation of psychological and care. The CALM approach is therefore promising in
social distress in patients with cancer and their families, terms of its focus on skills needed to provide patient-
and support for their personhood has been a central goal centred care. The psychological domains are presented
of palliative care since its inception.411 Palliative care in panel 10.
emerged, in part, in response to the neglect of the human
dimensions of suffering in modern medicine.412,413 Barriers and solutions
Nevertheless, much less attention has been paid to At present, the delivery of cancer care is more provider
training and the systematic delivery of psychological and centred than patient centred,426 and this situation applies
spiritual care in palliative care, as compared with physical to the system as a whole, including institutions, payment
interventions, for which there are well developed systems, infrastructure, and professional cultures. In

consequences, when these doctors are faced with clinical

Panel 10: Psychological domains of the Managing Cancer tasks such as discussing tumour-directed treatments with
and Living Meaningfully (CALM) approach a patient who has limited life expectancy or providing
Content care that includes death as the endpoint. Physicians
• Treatment decisions and communication with health-care commonly use euphemisms when topics are perceived as
providers challenging, often without checking if the information is
• Renegotiation of personal relationships and self-concept understood by the patient. This style of communication
• Reframing of priorities and the sense of meaning in life protects physicians from engaging in challenging
• Fears, hopes, and plans related to impending mortality communicative tasks because they do not have the skills
or the correct answer, despite the fact that open
negotiations with the patient would have been preferable.
sum, these factors are substantial barriers to making care Even if most patients with advanced cancer express a
more patient centred. preference for realistic information and discussions
In the public domain, the focus on promising new about treatment options and prognosis,357,429 barriers to
cancer therapies is prominent. This focus can be traced high-quality conversations exist on the patient’s side as
in present research priorities (see the section of this well. Patients might be reluctant to ask questions, express
Commission on societal challenges), and mirrors the their feelings, or admit they are insecure or do not
priorities and marketing activities of drug companies. quite understand the options and the implications.
The ultimate goal of contemporary science is said to be The patient’s use of two tongues—ie, one towards the
immortality,427 and, if correct, this goal is a strong driver oncologist the other towards other health-care
for further strengthening the focus on the tumour. These providers—is documented in a qualitative study of
factors also create expectations both within and outside patients approaching the end of tumour-directed treat
the medical community, and affects priorities at all levels ments.430 This complex communication points to a very
within health care and politics. Public opinion, and important and common trait among patients with
thereby the expectations of patients, contrasts with the advanced cancer: they are conflicted, both wishing to live
reality facing a substantial proportion of patients and as long as possible and wanting to live as good a life as
their families—ie, that their cancer is incurable. In our possible. This conflict is also commonly observed in
view, these factors, with their unilateral focus on the relation to wanting information about poor prognosis.
tumour, are barriers to a focus that includes both the There are examples of how the medical culture has
tumour and the patient. changed in response to new dogma. The best described
Oncology as a medical specialty has its roots in internal example is that discussed earlier: the change from hiding
medicine, while palliative care has its roots outside to disclosing the cancer diagnosis. In an editorial431
mainstream medicine. This difference in origin has commenting on Novack’s study,432 which confirmed
created cultures with different foci: the tumour and the disclosure to be the preferred practice, informed consent
host. A culture is characterised by sharing the same as a prerequisite or inclusion of patients into trials was
values, including taboos, and acts as an invisible but pointed to as the most possible explanation for the
commonly shared guidance for social interactions for change of attitude.
those sharing it.428 Bridging of the two cultures in When asked, doctors are generally positive about the use
oncology and palliative care is a challenge that is traceable of PROMs; this positivity is still much more common in
at all levels in health care, including daily activities at palliative care units than general oncology units, primarily
wards, departments, and hospitals. because of the enhanced focus on symptom management
A prominent characteristic of the medical culture has in palliative care. Frequently cited barriers to the use of
been the perception of the paternalistic doctor deciding PROMs are time constraints, cumbersome use, difficulties
on life and death. This was traditionally communicated related to interpretation, and logistical problems.380,433
at medical schools, and still fulfils the expectations of the Other factors, including resistance to change of an
students to some extent. Most students start at medical established system; absence of strong enough
school with an inner picture of the physician as the implementation; absence of economical or professional
person in power over life and death. For an educator, the incentives, or both; and absence of patient-centred focus,
most challenging parts of teaching communication skills also play a role. These factors are basically the same for all
to medical students are therefore motivating them for organisational changes, and are a challenge when all types
the training, and teaching them to systematically explore of new practices are implemented. Paradoxically, the
the perspective of the other—ie, the patient. introduction of new drugs or technologies does not seem
The tabooing of death is another observable trait of the to meet the same resistance to change. It is, therefore,
medical culture. The word death is seldom used,398 and reasonable to assume that the economic strength of the
many medical schools do not teach palliative care or end- producers of drugs and new technologies plays a role.
of-life care at all. The lack of exposure to these topics To enhance a patient-centred approach, the following
during the formative years as students has future factors apply at the organisational, professional, and

personal levels: implementation of a patient-centred

approach and communication plan into the SCPs; Panel 11: Patient-centred care—recommendations
willingness to change behaviour and incorporate this • Integrate patient-centred care (focusing on the host) as part of all cancer guidelines
into clinical practice; and a mutual understanding and and all treatment or care plans early in the disease trajectory until end-of-life care by
internalisation of the content and values of a patient- making societal and political demands at national and international levels, initiated by
centred approach among all health-care providers WHO and professional organisations and patient advocacy groups
involved in the care. • Implement routine use of patient-reported outcomes measures (PROMs) in all
The problems of information sharing within and settings of patient care by developing PROMs for use in electronic patient record
between health-care organisations have been recognised systems and assure that the information is used in the decision-making processes.
as a barrier to the implementation of ACP. Other barriers Implement incentive-driven indicators for the use of PROMs
include the competing demands of other work for health- • Integrate shared decision-making and advance care planning as a mandatory part of
care professionals, and the emotional nature of these all standardised care pathways by refining the methods for shared decision-making
types of conversations. Specially trained staff using a and advance care planning internationally, and adapting to national needs and norms;
structured approach has been shown to facilitate imple implement incentive-driven indicators for the use of shared decision-making and
mentation.434 Prompts in the electronic health record can advance care planning
increase the rates of documentation.435 At the patient • Involve and assess the family as a part of early integration of cancer palliative care by
level, factors influencing the uptake of ACP are complex, developing methods (tools) for involvement and assessment internationally, and
including previous illness experiences, preferences, and adapting nationally and implement indicators to monitor implementation
attitudes. Generally, patients with cancer are more open • Develop the content and basic method of standardised care pathway for use as a tool
to ACP than patients with non-malignant diagnoses;436 for early integration of palliative care into oncology care in hospitals and community
however, one systematic review371 suggested patients with care by encouraging international research on method development, complementary
cancer value the SDM and communication elements of intervention strategies and plans, training of health-care personnel, and resource set
ACP more than the avoidance of excessive medical with continuous funding
treatment at the end of life. • Mandatory training of oncology and palliative care specialists in patient-centred care,
Other strategies to enhance patient-centredness are including patient-centred communication by refining (and further developing)
elaborated on in other sections and include economic methods for training to be supplemented by international and national accreditations
incentives, organisation, and education. Recommendations
are presented in panel 11.
Although integration is important for all aspects of
Models of palliative care integration health care, it is of particular importance for patients with
The overall aim of integration of health-care services is to advanced cancer, who have complex problems that are best
coordinate care among providers and across settings, so managed by a multidisciplinary team.438 Within the
that patients and their families have access to the care they hospital setting, multidisciplinary teams can span various
need when they need it, resulting in improved health providers, including physicians (such as surgeons, patho
outcomes.42 Thus, a key question is: how should integration logists, radiologists, medical and radiation oncologists,
or collaboration occur between the two disciplines, and palliative care physicians) and other health-care
oncology and palliative care? Internationally, several providers (including pharmacists, social workers, occu
different organisational models have been developed, pational and physical therapists, spiritual care providers,
some of which have been tested in clinical studies. and music and art therapists). In addition, over the past
Although the content, structure (internally and externally), few decades, cancer care has become increasingly delivered
and professional competence within these models varies in outpatient, rather than inpatient, settings.35 For this
considerably, important common themes exist across the reason, primary care, including general practitioners and
models. The aim of this section is to present and discuss community nurses, are increasingly recognised to play an
models of care, and propose future organisational models. important role in cancer control, and communication
Over the past decade, several studies and models of care between multidisci plinary team providers across all
have addressed how the focus of palliative care can be settings and disciplines is recognised as necessary to
shifted from exclusively end-of-life to early integration improve patient care.439 The multidisciplinary team
within the cancer care trajectory. As highlighted in previous approach should, ideally, link oncology and palliative care
studies,3,5,47–51 early integration of palliative care improves services in hospitals, and involve and communicate with
quality of life, satisfaction with care, symptom control, primary health-care providers as needed. Consideration of
mood, and understanding of the illness. As a result, several how to optimally plan and collaborate between oncology
influential international organisations now endorse early and palliative care services should form an essential
palliative care as the standard practice of care for patients component of patient-centred care.
with advanced, incurable illness.15,86,437 The question is no
longer whether and why integration of palliative care is Models of integration—the broad picture
worthwhile, but how this can best be accomplished to Existing models of integration of palliative care into
optimise the goal of better patient-centred care. oncology care can be broadly classified as either

counterpoised with integrated care, in which palliative

Expertise in
palliative care care teams provide advice throughout the course of the
illness. Other conceptual models are provider based, and
classify palliative care, conceptually, as either primary
or secondary441 or primary, secondary, or tertiary442 on
Tertiary the basis of degree of complexity, and propose the
palliative care involvement of different care providers at each level
(figure 3). Although tertiary palliative care is consistently
depicted as being provided by specialised palliative care
Secondary palliative physicians, variations in the classification of primary and
care secondary palliative care exist. Primary palliative care is
provided by family physicians in some models443 and
oncologists in others.441 Some models specify that
secondary palliative care is provided by oncologists,444
Primary palliative care whereas others classify secondary palliative care as care
provided by palliative care specialists in non-tertiary
settings.443 These models emphasise differential
competence of providers in palliative care, with
Figure 3: Conceptual model of palliative care delivery based on provider expertise increasing levels of competence required to deal with
more complex issues.
The third conceptual model of palliative care integration
is setting based, in which delivery of care is based on the
setting in which care is provided. In these models, the
Inpatient palliative ideal setting for care is proposed to be in the community,
care with palliative care being provided primarily in the
patient’s home, rather than in the hospital (figure 4).440
This community-based care might be provided either by
the patient’s family physician, with support from a
Community- palliative care team,440 or by a specialist, community-
Home hospice based Outpatient palliative
care based palliative care team.445 The emphasis is placed on
palliative care
the facilitation of smooth transitions in care between
inpatient, outpatient, home, and community hospice
settings.
These conceptual models identify important factors
Inpatient hospice related to organisation, professional competence, and
timing as a part of the care pathway, which should be
considered when integrated oncology and palliative care
across all settings are described and defined. However,
no existing models specifically describe the detailed
mechanics of how patients move through primary and
Figure 4: Conceptual model of community-based palliative care provision
Adapted from Kamal and colleagues440 specialised levels of care or care settings, or how
communication occurs among providers. Furthermore,
conceptual or empirical. Conceptual models outline none of these models outline how care is provided within
broad theoretical principles, whereas empirical models the organisational structures of the oncology health-care
depict how these principles can be put into action in system. Full integration requires defined processes, such
specific settings. as clinical care pathways, referral guidelines, or pooled
The conceptual models can be classified broadly resources, to provide truly integrated care.42
into time-based, provider-based, and setting-based The remainder of this section will focus, in greater
models.148,440 The most well-known conceptual model of detail, on a provider-based conceptual model of primary,
palliative care integration is time based. This model secondary, and tertiary palliative care provision delivered
contrasts the traditional provision of palliative care only by generalists, oncology teams, and specialised palliative
at the end of life with a contemporary model in which care teams (figure 5).
palliative care is introduced at diagnosis, and gradually This model crosses settings and is not time specific,
increases until the time of death and bereavement but emphasises the need for oncology and palliative care
(figure 1). Non-integrated care, in which care is handed to be fully integrated across all settings and levels.
over to palliative care teams when the patient’s disease Through the use of standardised care pathways and
no longer responds to tumour-directed treatment, is referral guidelines, patients are more likely to be able to

access the right care, at the right place, at the right time.
This model is grounded in the concept that most
palliative care can, when the treatment goals are cure or Tertiary palliative care: palliative care Tertiary palliative care: available in all care
life prolongation, be provided by oncologists with basic specialists settings to support primary and
secondary providers
competence in palliative care. Palliative care specialists
should provide consultation for complex problems.7 We
review some examples of empirical models of palliative
Secondary palliative care: Standardised care Secondary palliative care: mainly in
care within each level of care of this larger model. oncology teams pathways, referral hospitals and in cancer centres
guidelines,
Primary, secondary, and tertiary palliative care and collaboration
integration
Primary palliative care Primary palliative Primary palliative
care: primary mainly in the
Primary palliative care has been defined as the core skills care teams community
and competencies that all clinicians should feel
comfortable providing to patients with advanced cancer
and their families. These skills include basic assessment Figure 5: Proposed model of optimal oncology palliative care provision, including integration across
and management of physical, psychological, social, providers and settings
spiritual, and practical problems; communication related Primary palliative care is community-based care provided by general practitioners, secondary palliative care is more
to prognosis and advance care planning; appropriate complex care provided by oncologists, and tertiary palliative care is complex care provided by multidisciplinary
specialist palliative care teams.
referral to available community-based supports; and
bereavement care for the family.7 Although primary
palliative care can occur at any clinical setting, it is best patients for the duration of their cancer treatment; this loss
provided in the community, both in outpatient settings of contact is often compounded by poor communication
for patients well enough to attend appointments, and in between cancer specialists and family physicians, making
the home setting. Home-based care is particularly it challenging for family physicians to re-engage with
important in this context, because it prevents unnecessary patients at the end-of-life, or to recognise when patients are
visits to the emergency department and hospital entering the final stages of their illness.439,458,459 Other
admissions, and enables death at home.446 barriers to the provision of primary palliative care include
Primary palliative care is best provided by multi time constraints,171,460,461 insufficient reimbursement,461 and
disciplinary teams that might include general practi insufficient palliative care training or expertise.62,462 Out-of-
tioners, home care nurses, personal support workers, hours support for community-based patients can be
and case managers.447 Although primary palliative care is particularly challenging.463 Home-based palliative care is
delivered by palliative care or hospice specialists in some often seen as labour intensive, poorly remunerated, and
countries, family physicians and general practitioners difficult to coordinate, especially outside of regular office
are well placed to provide primary palliative care. Their hours, or when family physician offices are far from their
therapeutic relationship with their patients and families patients’ homes.439,448,455
might span many years, giving them a unique perspective Multiple initiatives have enabled the provision of
into their patients’ values and priorities, potentially primary palliative care, both among family physicians
including preferences for end-of-life care and advance and in collaboration with secondary and tertiary palliative
care planning.448 A large proportion of patients with care providers. In some European countries (eg, Ireland,
cancer have uncontrolled symptoms from the time of the Netherlands, the UK, and Denmark), out-of-hours
diagnosis;449 thus, family physicians should be sufficiently cooperatives have been set up to lessen the burden on
competent to embark on an initial symptom management individual family physicians to provide round-the-clock
plan. As cancer progresses, patients often express a care for their patients;463,464 these cooperatives are generally
preference to receive care and to die at home, if possible,450 well received by patients and practitioners alike.465
which might be facilitated by primary palliative care Educational initiatives around the core skills of primary
providers.451 In addition, these physicians support palliative care at the level of the medical student and
families during bereavement, offering excellent con postgraduate learner are vital, as are continuing medical
tinuity of care that is highly valued by patients and their education programmes, as discussed in the section of
families.452 The engagement of family physicians and this Commission on education. The development of
general practitioners in palliative care varies widely: from collaborative partnerships between primary and tertiary
less than 50% in some countries, such as Canada and palliative care providers is recognised as a vital component
Japan,453,454 to up to 85% in the UK, the Netherlands, and of the promotion and support of primary palliative care,448
Australia.455–457 as discussed later.
The literature on the integration of primary palliative In the Netherlands, the general practitioner and home
care into oncology is limited. As cancer care becomes more care nurse are the main providers of care for
specialised, many family physicians lose contact with their community-dwelling patients with cancer and palliative

care needs. Over the past 10–15 years, nurse case appropriate palliative care.176 An additional complicating
managers have been introduced in some areas. To ensure factor might be that some patients prefer to receive more
continuity of care, the case manager collaborates with the positive messages from their oncologist regarding their
patient, their informal carers, and the medical cancer, linking this with a greater compassion on the
professionals involved in their care (ie, general part of the physician.470
practitioner and oncologist). The case manager provides In an effort to improve integration and promote both
advice to patients and their informal carers, and refers secondary and tertiary palliative care provision, ESMO
them to other care providers as necessary. The case has developed designated centres of integrated oncology
manager might also offer palliative care advice to other and palliative care on the basis of 13 rigorous criteria
health-care providers, including the general practitioner across clinical, research, and educational domains.86
and the home care nurse.466 A 2017 survey of all active ESMO-designated centres
identified high levels of routine symptom screening and
Secondary palliative care goals of care discussions among oncologists, although
Secondary palliative care refers to the care provided by less attention was paid to advance care planning and end-
the oncology team in the specialist health-care system to of-life discussions, which were more likely to be
both inpatients and outpatients. Because oncology teams addressed by the palliative care services.155
are based in hospitals and cancer centres for the most
part, these are the main settings for secondary palliative Tertiary palliative care
care. Cancer care itself is multidisciplinary, and involves Tertiary palliative care is provided by physicians and other
specialists from medical, radiation, and surgical multidisciplinary team members with specialist palliative
oncology, as well as specialised nurses, social workers, care training. These teams might include specialised
psychologists, psychiatrists, dietitians, physiotherapists, palliative care physicians, nurses, social workers, spiritual
and occupational therapists, among others.467 All of these care providers, occupational and physical therapists,
people require core clinical competencies in palliative and pharmacists, among others. Clinical guidelines
care, as described later. recommend that inpatients and outpatients with advanced
Important strides have been made in the promotion of cancer or high symptom burden, or both, should receive
secondary palliative care as a part of oncology care dedicated palliative care services early in the disease
programmes. ASCO has formally endorsed early palliative course concurrent with cancer treatment.15 However, with
care,15 and has published several clinical guidelines for shortages of tertiary palliative care specialists worldwide,
palliative care in oncology.7,468 Several other international limiting the provision of tertiary palliative care to the
bodies have made efforts to formalise the role of subset of patients whose care needs are the most complex
oncologists in providing secondary palliative care. Among and are not adequately met by primary or secondary level
these efforts is a partnership between ASCO and the providers is more practicable. It is therefore important to
American Academy of Hospice and Palliative Medicine, have mechanisms to determine which patients would
which has produced a consensus statement using a Delphi benefit most from consultation with tertiary palliative care
process on high-quality palliative care delivery in US services.471
medical oncology practices469 (panel 12). In this statement, Tertiary palliative care should be available to all patients
they recommend that oncologists should provide regular with cancer, regardless of prognosis, and to primary and
systematic symptom assessment at least monthly, and a secondary palliative care providers on a consultant basis
basic assessment of psychosocial wellbeing, faith group, in all settings, including for inpatients, outpatients, and
and caregivers for distress if they accompany patients to in the community. In settings in which resources are
the appointment.469 Secondary palliative care also includes limited, palliative care services provide care mainly as
communication of prognosis to the patient and primary consultation services for inpatients.119 Acute palliative
care provider, and assessment of prognostic understanding. care units for the specialised management of complex
Patients with complex or uncontrolled symptoms should symptoms and psychosocial concerns are limited to a
be referred to tertiary palliative care services as available.469 minority of tertiary care hospitals and hospices.438 In the
Despite these guidelines, oncologists continue to community, long-term palliative care units, hospices,
vary in their perceptions of their role in providing and palliative care home consultation services provide
secondary palliative care. Some provide no palliative care valuable support to patients at the end of life. Over the
and refer all patients to tertiary services; some see past few years, full integration, especially for patients at
themselves as solo providers of simultaneous oncology earlier stages of their illness, has been recognised as
and palliative care, and do not refer to tertiary palliative possible only through an outpatient palliative care
care; and others refer to tertiary services only in programme.35,171,472 Development or expansion of tertiary
complex clinical situations.171 At the secondary palliative palliative care services should consider the unique needs,
care level, patients might associate cancer treatment philosophy, and culture of the broader institution, with
directly with hope, and a singular interest in pursuing input sought from key stakeholders across clinical and
active anticancer treatments can affect the delivery of managerial levels.473

Panel 12: Essential elements of secondary palliative care in oncology practices

Symptom assessment and management Advance care planning
• Monthly symptom assessment using a validated • Begin advance care planning at the diagnosis of advanced
quantitative instrument cancer, starting with assessing the patient’s and family’s
• Educate patients about the cause and management of readiness to discuss advance care planning and any concerns
existing symptoms they might have
• Instruct patients how and when to contact the clinic during • Code status (ie, the type of resuscitation procedures requested
and after hours for new or worsening, or poorly controlled, by the patient), living wills, advanced directives, health-care
symptoms surrogate, and out of hospital do not resuscitate orders should
• Assess the effectiveness of adjusted medication by the next be discussed, completed and documented as soon as possible
clinical encounter
Coordination and continuity of care
Psychosocial assessment and management • Coordinate care with primary care, hospice, hospital, and
• Conduct an initial, basic psychosocial assessment nursing home
• Assess distress with a validated quantitative instrument
Appropriate palliative care and hospice referral
initially and after any clinical change (eg, cancer progression)
• Describe the difference between hospice and palliative care
• Manage distress at a basic level with supportive, empathetic
to patients and families as soon as possible after an
statements and validation of the patient’s experience,
advanced cancer diagnosis
otherwise patients should be referred
• Conduct routine patient assessments to determine the need
Spiritual and cultural assessment and management for palliative care or hospice referral
• Document patient’s faith • Refer patients with a prognosis of 3 months or less, or an
• Provide patients with a framework to consider their goals Eastern Cooperative Oncology Group performance status of
and hopes along with the probable medical outcomes of 3–4 to hospice, or both
their illnesses and support those goals • Collaboratively agree on referrals with the patient or family,
• Assess and document preferences for communication and or both
language
Carer support
• Provide translation services
• Obtain permission to speak with primary caregivers and to
Communication and shared decision-making include them in conversations about the patient’s care
• Assess patients and families for preferences for how they • Assess caregivers attending clinic visits with patients for
want to receive information regarding the patient’s cancer, distress at least once
prognosis, treatment risks and benefits, treatment plan, and • Inform caregivers how to contact the clinic in routine and
bad news, and who participates in the decision making and emergency situations
to what extent • Provide information about local and online caregiver
• Provide oral and written documentation of the treatment resources
plan to the patient and family, with specific details regarding • Provide bereavement follow-up in the form of a phone call
expectations for disease control, effects on symptoms and or condolence card, or both, and information regarding
quality of life, length and frequency of treatment, and the local bereavement resources
frequency of and rationale for disease reassessment
End-of-life care
• Assess the patient’s and family’s understanding of the
• Have processes to evaluate patient symptoms, advise
patient’s illness, prognosis, and goals of care at diagnosis,
medication changes to patients and family, and provide
disease progression, and with changes in the treatment plan
on-call coverage 24 h per day, 7 days per week
• Openly acknowledge and address mistakes as soon as they
are noticed Panel adapted from Bickel and colleagues.469
How should tertiary palliative care be integrated? there are few consultations. However, outpatient
Availability of tertiary palliative care for outpatients is of palliative care clinics are more efficient on a larger scale,
paramount importance for integration into standard and allow patients to be seen by several multidisciplinary
oncology care, because most oncology care, including for team members working together in the clinic.472,476,477 The
patients with advanced disease, occurs on an outpatient most robust evidence for early palliative care is for
basis. Several models of outpatient tertiary palliative care palliative care clinic interventions, and has shown that
have been proposed, including mobile teams, free these clinics improve quality of life, symptom control,
standing palliative care clinics, and embedded clinics.474,475 and mood.3,5,63 Embedded clinics offer opportunities for
A mobile team, where outpatient palliative care con oncologists and palliative care clinicians to collaborate
sultations in oncology clinics are done by the inpatient and coordinate care, and allow rapid access to palliative
consultation service on a same-day basis, is feasible if care teams. However, this model presents challenges,

Cancer Control aims to address this issue, identifying

Referral to oncology palliative care clinic palliative and supportive care as one of the four essential
pillars of cancer treatment and care (along with cancer
Oncology palliative care clinic consultation Early palliative care
data for public health, early detection and diagnosis, and
timely and accurate treatment).485 ESMO-designated
centres also strive to boost the status of integrating high-
Longitudinal follow-up in tandem with quality palliative care services within oncology.438,486
oncology, primary, and community care for:
• symptom control
Closely connected to this is the problem of adequate
• psychosocial care funding to support integration. Although oncology
• referral to community services leadership tends to agree that integration is beneficial,
• advance care planning
funding to support programme expansion often lags
behind. A survey of members of the Multinational
Association of Supportive Care in Cancer, the European
Community palliative Acute palliative care Home palliative care Transitional and Association for Palliative Care, and ESMO found that
care unit or residential unit end-of-life care only 17% of respondents felt their institution was likely to
hospice
increase palliative care funding; 49% felt it was unlikely
their institution would increase inpatient palliative care
beds; and respondents were neutral regarding future
Figure 6: Tertiary palliative care on the basis of referral to a palliative care clinic
palliative care team hiring plans.438 Despite several
Referrals are made by the patient’s oncologist. Care is integrated and collaborative across acute and community
care settings. Ultimately, care is transferred to home, hospice, or a palliative care unit. Figure adapted from Hannon studies137 demonstrating the cost-effectiveness of
and colleagues.472 palliative care teams, cost-effectiveness does not seem to
factor into budgetary considerations at the oncology
including finding adequate clinic space, fatigue on the level.
part of patients with longer clinic visits, and involvement A shortage of trained medical and nursing personnel,
of only one discipline—usually a single physician or and poor reimbursement for palliative care physicians
nurse.148 have also been cited as barriers to the access and
Several models of integrated tertiary palliative care development of tertiary palliative care, even within cancer
programmes have been described. In 1995, the palliative centres and ESMO-designated centres of integrated
care programme in Edmonton, Canada, was one of the oncology and palliative care.438 At the individual oncologist
first to report their practice, which consisted of an level, substantial heterogeneity remains in referral
inpatient palliative care unit housed within an acute practices to tertiary palliative care teams because of factors
hospital setting, as well as a consultation service and an ranging from personal opinions to structural issues. For
outpatient clinic. From the outset, a strong emphasis was some oncologists practising secondary palliative care,
placed on the use of standardised assessment tools, wide- especially in community practice, the additional reim
ranging education and research initiatives, and close bursement afforded by this might limit their willingness to
integration with family physicians to enhance primary fully integrate with palliative care teams or refer to tertiary
palliative care provision.478,479 These elements of care were palliative care services.438 In an effort to standardise referral
similarly emphasised in subsequent reports of successful practices, the use of specific criteria to trigger automatic
tertiary palliative care programmes in Lausanne,480 referral to palliative care teams alongside concurrent
Milan,481 Cleveland,482 Houston,483 Trondheim,47 and oncology care have been proposed; the success of these
Toronto,484 with the Trondheim and Toronto programmes criteria has yet to be explored.35
also publishing successful randomised controlled trials Ongoing stigma and misconceptions about the term
illustrating the effectiveness of this model of care.5,47 The palliative care are frequently quoted as barriers to
model of palliative care at the Princess Margaret Cancer integrated services.487 Because of its historical association
Centre, Canada, serves as one empirical example and is with end-of-life care and medical futility, the name itself
described in figure 6. is often cited by oncologists and patients as an obstacle to
early referral164 (see the section of this Commission on
Barriers to integration of tertiary palliative care societal challenges). In one centre, the outpatient
Several areas are consistently identified as barriers to palliative care service has been renamed supportive care,
fully integrated oncology and palliative care services, which has been associated with earlier referrals.488
across system, organisational, and clinical levels. An
absence of institutional recognition of the value of Human resources and clinical competencies
tertiary palliative care services has limited the develop To deliver high-quality, integrated palliative care, an
ment of new services. Palliative care services are interdisciplinary approach is required. The competence
infrequently afforded the same priority as other areas of of palliative care needs to be placed into context in the
cancer detection and treatment at executive or managerial cancer plans, such as participation in the multidisciplinary
levels. A new initiative from the Union for International teams as active and integrated partners. As mentioned

earlier, the multidisciplinary team includes not only Care transitions and collaboration: moving among
physicians and nurses, but also social workers, spiritual levels of care
care providers, physiotherapists, occupational therapists, Several common facilitators to successful integration
psychologists, psychiatrists, and pharmacists, among across primary, secondary, and tertiary palliative care
others. Inclusion of these skills can be provided by the have emerged, including structures and tools for
palliative care specialist physician, on the basis of the transitions between levels of care and collaboration
needs addressed by the multidisciplinary teams. Access among disciplines. Although there might be some
to and close links with community-based nursing and overlap of roles, clarity and clear division of each team’s
allied health-care providers is also essential to ensure respective responsibilities is necessary to ensure a
seamless transitions between care settings. consistent message for patients.171,492,493
In terms of clinical competencies, primary palliative Referral guidelines or other types of predefined
care providers should have core skills in assessing and structures, such as palliative care incorporated in the
managing physical and psychological symptoms, as well SCP in detail, can help to clarify which patients and
as knowledge to use SDM in daily clinical practice, which when these patients are likely to benefit from referral to
also includes ACP for patients with short life expectancy tertiary palliative care services. In a recent study471 using a
and planning, coordinating, and providing end-of-life Delphi process, international palliative care experts
care in patients’ homes when feasible. reached consensus on 11 major criteria for outpatient
Core teaching on pain and symptom management, and palliative care referral in cancer centres, on the basis of
end-of-life care has been recommended for medical stage of disease, prognosis, and clinical problems. These
students in the UK and the USA;489,490 initiatives such as criteria were categorised into needs-based and time-
the Canadian Learning Essential Approaches to Palliative based criteria (panel 13).471 The palliative care experts For the Canadian Learning
and End-of-life Care (LEAP) programme provide reached consensus on referrals based on both automatic Essential Approaches to
Palliative and End-of-life Care
multidisciplinary primary palliative care training for all referral and clinician-based referral, with only 7%
(LEAP) programme see
health-care providers (see the section of this Commission agreeing that referral should be based on automatic http://pallium.ca/
on the role of education). referral alone.494 These criteria can be used as guides
For secondary palliative care, wide variations exist in when detailed SCPs are developed in oncology.
terms of the training and competencies of individual SCPs have been suggested as a potential means of
oncologists, which is often a result of the clinical setting recognising transition points in care and ensuring high-
within which they work. Many physicians working within quality care regardless of the clinical setting. In Canada,
designated centres of integrated oncology and palliative Cancer Care Ontario has developed collaborative care
care are dual-certified in both oncology and palliative plans based on Palliative Performance Status (PPS) for
care (65% in a 2017 study).155 These centres were also stable (PPS 70–100), transitional (PPS 40–60), and end-
more likely to have access to a broad range of of-life (PPS 0–30) stages. Lessons learned from the use
multidisciplinary clinicians.155 Mandatory rotations in of SCPs in end-of-life settings indicate that these
palliative care and modules in symptom management,
communication skills, and updated skills in SDM and
ACP have been recommended to improve secondary Panel 13: Models of palliative care integration
palliative care competencies. At minimum, competencies Needs-based
should include basic assessment of pain and other • Severe physical symptoms (eg, pain, dyspnoea, or nausea
symptoms; assessment of psychosocial, spiritual, and scored 7–10 on a ten-point scale)
cultural needs for the patient and family; appropriate • Severe emotional symptoms (eg, depression, or anxiety
goal-based communication; skills in using SDM and scored 7–10 on a ten-point scale)
ACP; and coordination of end-of-life care. • Request for hastened death
Tertiary palliative care services should be led by • Spiritual or existential crisis
clinicians with specialist palliative care training and • Assistance with decision making or care planning
certification where available. As of today, most countries • Patient request
with such a certification have organised it as a dual • Delirium
certification. For cancer centres, specialist certification in • Brain or leptomeningeal metastases
both oncology and palliative medicine is necessary (see • Spinal cord or cauda equina compression
the section of this Commision on education). As
consultants, these clinicians should have appropriate Time-based
training in the management of complex symptoms • Within 3 months of diagnosis of advanced or incurable
and problems throughout the disease course and cancer for patients with median survival of 1 year or less
bereavement. Palliative care is now recognised as a • Diagnosis of advanced cancer with progressive disease
medical specialty or subspecialty across 18 European despite second-line systemic therapy (incurable)
countries as well as the USA, Canada, and Australia.491 Panel adapted from Hui and colleagues.471

pooling resources, especially in the early stages of

Panel 14: Models of integration—recommendations palliative care programme development.
• Establish integrated specialised palliative care or oncology Collaboration can also be facilitated by technology and
services, or both, at cancer centres by developing clinical tools. Symptom screening has been established
integrated models, training personnel, making palliative as a standard of care in all cancer centres in Ontario,
care mandatory at the multidisciplinary teams, and giving Canada,498 and proven to be effective in routine oncology
economic incentives practice75,499 and in pilot projects in primary care
• Establish multidisciplinary community teams for early practices.500 This collaboration can serve to encourage
integration by developing models for community teams systematic assessment and management of symptoms
and evaluating the models in research projects by oncologists, and trigger timely referral to tertiary
• Integrate community-based and hospital-based services palliative care programmes. Joint electronic patient
by establishing formal contracts on integration and records or mutual access to patient records, among all
payment plans (resource setting) levels of care providers, can improve information transfer
• Embed basic early palliative care into oncology among care providers in the hospital and community.501
programmes by making palliative care a mandatory part Telehealth is also being explored as an intervention to
of oncology training, and revising national content of improve communication in palliative care, particularly
oncology training programmes and give international for people living in rural regions.502
recommendations
Conclusion
We have presented conceptual models of palliative care
pathways should be detailed while also flexible in integration, as well as principles, competencies, and
addressing individual needs; not be a substitute for resources necessary to achieve integration in various
empathic care of the patient; and be coupled with ACP, settings. There is no single model of palliative care
comprehensive education, and training in palliative integration that is tested in clinical studies or used in all
care.495,496 Further research is needed to assess the health-care systems. This heterogeneity can indicate that
effectiveness of these pathways in earlier stages of palliative care integrated in oncology is in its infancy. The
disease.187,497 need to agree, on the basis of high-quality studies, on
The development of strong, collaborative relationships models that fit the different health-care systems in
among primary, secondary, and tertiary providers are countries of high and middle income is urgent. The
essential for truly integrated care. Among primary and overall goals of such a discussion are that these novel
tertiary palliative care providers, strategies could include organisational models will meet the needs of all patients
mentorship and advisory programmes facilitating ready in all settings and circumstances. However, a successful
access to tertiary palliative care teams, including out-of- model of integration needs to incorporate primary,
hours support; inviting primary palliative care providers secondary, and tertiary providers; span the inpatient,
to engage in discharge planning discussions or family outpatient, and community settings; and specify how
meetings for shared patients before home discharge; movement between these levels occurs in a systematic
and maintaining excellent communication between fashion. Although sound evidence exists for the
community-based and hospital-based teams through involvement of early tertiary palliative care for patients
shared electronic records. These partnerships could help with advanced cancer, little exists for models of primary
to improve family physicians’ confidence in providing and secondary palliative care provision, and for care
primary palliative care and in recognising transitions in pathways bridging levels of palliative care. Research in
care.448 these areas should be prioritised. Recommendations are
Collaboration between secondary and tertiary palliative presented in panel 14.
care providers in cancer centres should be a part of the
multidisciplinary teams, encouraged by joint rounds and The role of education: challenges and
tumour boards, and supported by combined palliative recommendations
care and oncology educational activities for trainees.44 Several of the previous sections have highlighted the need
Shared support staff (eg, allied health professionals or for education of health-care providers as a key factor for
nursing staff) can act as a bridge between services.171,493 the promotion of integration of oncology and palliative
Joint patient consultations, proximity of palliative care care, both on the clinical and organisational levels. This
clinics to oncology clinics (or palliative care clinics is in line with recommendations from experts,
embedded into oncology clinics), and the involvement of stakeholders, and professional health organisations.44,503,504
palliative care teams in tumour boards or cancer At present, the need for basic and specialist competence
committee meetings might be superior to communication in palliative care is unmet at all levels of health care,
via email or phone.171,492 In addition to the clinical which calls for increased educational efforts.
advantages offered by such collaborative models, there Integration of oncology and palliative care requires close
are also potential financial advantages associated with collaboration and exchange of information between

primary, secondary, and tertiary palliative care providers

(see the section of this Commission on models). Tertiary Panel 15: Three levels of palliative care
palliative care specialists are often located in comprehensive Basic
cancer centres or university hospitals, and are commonly (Level A; undergraduate and postgraduate)
also engaged in academic activities such as research and Integrate palliative care methods and procedures in general
education. The skill set of tertiary palliative care specialists care, for all health-care professionals
is essential to support primary and secondary providers.
These premises expand the responsibilities of tertiary Advanced
palliative care beyond the cancer centre setting through (Level B; postgraduate)
education and mentorship programmes aiming to upskill For professionals involved with palliative care, but not as
primary and secondary health-care providers. their main occupation (eg, oncologists)
The heterogeneity of the organisational models Specialist
described in the section of this Commission on models (Level C; postgraduate)
does not allow for conclusions to be drawn about the For professionals working solely in palliative care whose main
kinds of competence and skills that best promote activity is complex problems requiring specialised skills and
integration. We were unable to identify reports, policy competencies
statements, or articles at an international level that
specifically addressed how education programmes can
promote integration of oncology and palliative care, or management, and one was a systematic review about
what they should include, except for general statements early integration.
about palliative care.
In this section, we therefore describe available Educational strategies
international educational strategies and recommen International agencies and professional associations
dations in palliative care, contents of oncology and have developed and promoted policies and projects,
palliative care curricula, and educational barriers and including educational strategies and recommendations,
facilitators. We also discuss how education can promote to improve palliative cancer care. WHO has recognised
integrational models. Medical education from under that national actions are necessary to strengthen palliative
graduate to postgraduate levels is the primary focus of care education, and that such action should be “ensuring
this section, with the awareness that palliative care shall that education about palliative care (including ethical
be delivered by multidisciplinary teams that include aspects) is offered to students in undergraduate medical
health-care providers with qualifications in disciplines and nursing schools and health care providers at all
other than medicine. Expanding the panel to the levels, in accordance with their roles and responsibilities
education of all the other important health-care providers and as part of human resource development”. EAPC has
in the multidisciplinary team would exceed the limits of launched a recommendation of three levels of palliative
this section. With a focus on medical education, care education that can serve as a basis for integration507,508
principles and content are also considered of value for (panel 15). Another example of an integrative approach
education of other health-care providers. originates from ESMO, which has developed designated
This section is based on available information on centres of integrated oncology and palliative care on the
palliative care education (specialisation and postgrad basis of rigorous criteria across clinical, research, and
uation programmes), such as the supplement to the educational domains, promoting both secondary and
EAPC Atlas of Palliative Care in Europe,491 EAPC Atlas of tertiary palliative care provision. To date, close to
Palliative Care in Latin America,505 and the website 200 centres from 41 countries have achieved this
Global Directory of Education in Palliative Care of the designation.
IAHPC.506 Further information was gathered from
medical society papers, websites supplemented by a Accreditation of palliative medicine
systematic review of literature using the MESH terms In general, certification in palliative medicine falls into
palliative or palliation, oncology or cancer, and three categories, depending on the postgraduate
education, and the words integration or integrative in educational system of the different countries: specialty,
the title or abstract. The search yielded 23 articles subspecialty, and general competence in the field. All
considered of relevance for this section. Of those three categories require a basic medical degree; however,
articles, 12 were informative articles (consensus, panels, subspecialty in palliative medicine also requires a clinical
indicators, recommendations, discussion, debate, or specialty degree in another medical area. Certificate of
state-of-art) regarding integration of palliative care and competence refers to formal educational courses in
oncology); four were descriptions or evaluations of palliative medicine approved by national health
multidisciplinary curriculum or specialist education, authorities and medical societies, but not necessarily a
four presented professional perspectives or opinions, recognised new specialty in some countries.491 The
two surveys focused on guidelines and service supplement of the EAPC Atlas of Palliative Care in

Accreditation Denomination in English Clinical practice Theoretical training Research

(years)
Australia and Specialty Palliative medicine (medical specialty) 3 ·· One to three projects
New Zealand
Canada Subspecialty Subspecialty of palliative medicine 2 350 h One project
Czech Republic Subspecialty Palliative medicine 1 12 months ··
Denmark Special denomination Competence in the field of palliative medicine 2 6 weeks One project
Finland Special denomination Special competence in palliative medicine 2 150–270h One project
France Special denomination Diploma of complementary specialised studies in pain 2 170 h One project
medicine and palliative medicine
Georgia Subspecialty Palliative care and pain medicine 0·5 75 h ··
Germany Subspecialty Palliative medicine 1 40 h Not required
Hungary Subspecialty Subspecialty in palliative medicine 1 80 h ··
Ireland Specialty Certificate of completion of training as specialist in 4 Varying between different Not required
palliative medicine universities
Israel Subspecialty Palliative medicine subspecialty 2 ·· ··
Italy Special denomination Master’s programme in palliative care for specialist 0·5 1500 h One project
physicians
Latvia Special denomination Special competence in palliative care 2 400 h 80 h
Malta Specialty Palliative medicine Most training Most training acquired Not required
acquired abroad abroad
Norway Special denomination The formal competence field of palliative medicine 2 180 h One project
Poland Specialty Specialisation programme in palliative medicine for 2 ·· One project
physicians
Portugal Special denomination Palliative medicine competence 1 400 h Three projects
Romania Subspecialty Diploma of complementary studies in palliative care 0·25 2 months ··
Slovakia Special denomination Specialisation study in the field of palliative medicine 0·5 ·· ··
Sweden Subspecialty Subspecialty in palliative medicine 2·5 120 h Not required
UK Specialty Certificate of completion of training as specialist in 4 Varying between the Not required
palliative medicine different universities
USA Subspecialty Hospice and palliative medicine certification 1 Varying between the different Varying between the different
universities and states universities and states
Table adapted from Bolognesi and colleagues509 and Centeno and colleagues.510
Table 6: Accreditation of palliative medicine education
Europe491 collected information on education and requiring a minimum of 3 to 4 years of postgraduate

certification in palliative care from 18 European training to achieve certification. In other countries (eg,
countries, Australia, Canada, and the USA. As expected, Canada, the USA, France, and Germany), palliative care
type of certificates, demand for clinical practice, is organised as a medical subspecialty.514,515 Other
theoretical content and length, and whether research was educational programmes are directed towards medical
a mandatory component all varied (table 6). specialists associated with some kind of accreditation,
The integration of palliative care into oncology might which include the Japanese Palliative Care Emphasis
be highly dependent on the level of accreditation. Thus, Program on Symptom Management and Assessment for
the different models of integration generally originate Continuous Medical Education (PEACE)515,516 and The
from countries with some kind of accreditation of Nordic Specialist Course in Palliative Medicine.517 The
palliative medicine and availability of tertiary palliative Nordic Specialist Course in Palliative Medicine is a joint
care. Palliative medicine achieved specialty or sub venture between the Associations for Palliative Medicine
specialty status in the UK in 1987, the USA in 2006, and in the Nordic countries (Denmark, Sweden, Norway,
Canada in 2016.511,512 Palliative medicine has also been Finland, and Iceland), and has resulted in a theoretical
established as a specialty in multiple countries in the specialist training course in six modules over 2 years,
Asia-Pacific region, including Australia, New Zealand, combined with a clinical stay at a specialised palliative
China, Japan, Taiwan, Malaysia, Singapore, and India.513 care unit. However, palliative medicine was accredited
Other countries in Europe, Asia, Latin America, and as a special competence in Finland in 2007, and a
Africa are actively working toward accreditation. In some subspeciality in Sweden in 2015.491
countries, such as the UK, Ireland, New Zealand, and The heterogeneity in specialty status without clearly
Australia, palliative care is a full medical specialty, defined competencies for palliative care physicians is

probably associated with variability in the content and

Levy et al Gamondi et al Hui et al (2015);44
quality of care delivered, and is a challenge for the (2014)468 (2013)508 Hui and Bruera
advancement of clinical palliative care. Furthermore, (2015, 2016)35,148
the classification and definitions of speciality and Palliative care in undergraduate curricula Y Y Y
subspeciality differ considerably between countries, as Lectures and curricula on palliative care for Y ·· Y
can be seen from the clinical practice and theoretical oncology professionals
training section of table 6. A substantial proportion of Oncology rotations for palliative care fellows Y ·· Y
those attending the programmes are oncologists who Palliative care rotations for oncology fellows ·· ·· Y
have been recruited for the subspecialty model for Conferences on palliative care for professionals Y ·· Y
palliative medicine, which might enhance integration. Continuation education for practicing oncology Y Y Y
professionals
Palliative care and oncology curricula for physicians Palliative care skills formal examinations Y ·· Y
Several documents specify a framework for competence Combined palliative care and oncological ·· ·· Y
for physicians, developed by their respective national educational activities for fellows and trainees
medical associations. Our literature review showed that Post-graduation in palliative care ·· Y Y
education in palliative medicine is generally Y=strategy suggested.
recommended to be included in undergraduate and
postgraduate curricula, updated by continuing education, Table 7: Suggested educational strategies to improve competences
lectures, courses, and conferences. The EAPC Steering
Group on Medical Education and Training published
Panel 16: Main objectives of the recommendations for a global core curriculum in
prototypes of postgraduate and undergraduate curricula
medical oncology
for palliative medicine in 2009, and 2013.518,519 In addition,
rotation of trainees and fellows is common, and is • To screen, assess, prevent, and manage symptoms of patients with cancer such as
designed to promote integration35,148,468,508 (table 7). Thus, pain, fatigue, anorexia, anxiety, depression, breathlessness, and nausea
curricula in palliative medicine might facilitate • To communicate effectively with patients and families about understanding of and
integration of oncology and palliative care from an early coping with cancer, prognosis, difficult decisions, end-of-life and its preparation,
stage in the education process.520 EAPC recommends including psychosocial and existential dimensions
curricula at medical schools should cover six domains, • To recognise the role of cancer rehabilitation, including physical therapy and nutrition
achieving six overall learning goals.520 Recommended • To recognise the importance of culturally competent, multidisciplinary care that also
educational goals include experiential learning, active includes the families
techniques, multiprofessional learning, and experience • To understand how to integrate palliative interventions in routine multidisciplinary
in palliative care, and must cover more than 40 hours cancer care
in total. The topics should be included in examinations, • To recognise the difference between burnout, compassion fatigue, and depression
teaching should be done by palliative care specialists • To ensure timely referral to specialist palliative care teams
and professional groups other than doctors (eg, nurses,
psychologist, and chaplains), and ethical and, psycho
logical social, and existential issues should be integrated superior vena cava obstruction, and hypercalcaemia.
into the curricula. Additionally, education in palliative Knowledge about prognostication of different cancer
care should be removed from oncology and diseases, chemo therapy lines, and radiation therapy
anaesthesiology, and taught as an independent subject. should also be implemented in the curricula. At present,
Bolognesi’s survey509 addressed various subjects no overall recommendations on the exact amount of
present in the postgraduate palliative care specialisation oncological teaching in postgraduate palliative care
programmes in Europe, including pain and symptom accreditation programmes exist, and the actual amount is
management, pharmacology of opioids and other essential probably highly variable in different countries.
drugs, psychosocial issues, ethical issues, communication, ASCO have deliberately included current best evidence
teamwork, organisation of delivery of care, end-of-life care, of palliative care in oncology curricula, aimed at
normative and legal issues, oncology, non-malignant enhancing oncologists’ understanding of the basic
diseases, supplement by community palliative care, principles of palliative care, while acknowledging that
culture, language and religion, grief and bereavement, and complex scenarios and refractory suffering should be
applied teaching from other disciplines, including referred to palliative medicine specialists.15 The third
radiology, psychiatry, and public health. Specialist palliative edition of the Recommendations for a Global Core
care curricula should provide sufficient theoretical and Curriculum in Medical Oncology, published in 2004,
practical knowledge and skills to handle oncological and updated in 2010, and 2016,521 outlined specific
emergencies, including clinical detection, emergency competencies for oncologists related to supportive and
management and referral to specialists for spinal palliative care and was endorsed by ASCO and ESMO
cord compression (eg, radiotherapy and neurosurgery), (panel 16). At present, no overall data on the amount of
pathological fractures, raised intracranial pressure, palliative care teaching in postgraduate oncological

accreditation programmes exist, and the actual amount These workforce-related issues are substantial barriers
is probably highly variable in different countries. because palliative medicine is the fastest growing medical
The NCI has developed the Education in Palliative and specialty or subspecialty worldwide.529 These issues are
End-of-Life Care for Oncology (EPEC-CO) curriculum—a not only related to low staffing levels, but also to the level
multimedia curriculum that can be used as a self-study of competences and practical skills, inadequate training
tool or presented by seminar or webinar.522 The in communication, insufficient knowledge about the
Northwestern University Feinberg School of Medicine quality of the health-care delivered by other professions
offers the train-the-trainer EPEC courses to facilitate or specialists, and resistance to refer patients to
dissemination of the curriculum via certified EPEC specialised palliative care or hospices.444,530,531 Therefore,
trainers.523 The Accreditation Council for Graduate expansion and support of educational programmes for
Medical Training in the USA has also mandated newly educated and midcareer physicians are crucial to
competency in hospice and palliative care for medical meet the workforce shortage in palliative medicine.527
and haematological oncology fellowship programmes.461 Although proposals exist on how to develop and
In addition, educational curricula have been organised enlarge the contents of curricula for oncologists and
as the LEAP and LEAP Oncology programme and the for palliative care specialists at different levels of
Virtual Learning Collaborative, a web-based education specialist education, budget constraints and absence
module under development by ASCO and American of administrative support can hamper the development
Academy of Hospice and Palliative Medicine.524 Moreover, of educational and training programmes intended to
US and European organisations, such as the National enhance integration. Despite the fact that Europe is
Comprehensive Cancer Network (NCCN) and ESMO, considered the pioneer region of palliative care,
have published clinical practice guidelines on palliative a descriptive EAPC study532 of undergraduate medical
care.325,468,525,526 These initiatives are a step towards the education in Europe (43 countries) identified low
integration processes. Moreover, an international Delphi investments in education. Palliative medicine was taught
survey44 identified four major educational strategies in medical schools in only 13 (30%) countries and was a
related to postgraduate oncology programmes: a didactic compulsory course in six (14%) countries, with only
palliative care curriculum for oncology fellows provided 17 (40%) countries having a full professorship in palliative
by palliative care teams, continuing medical education in medicine.532 The study did not explore the reasons for
palliative care for attending oncologists, combined these low numbers. Knowledge of oncology and palliative
palliative care and oncological educational activities for care congruent with the level of care that is given
fellows and trainees, and routine rotation in palliative constitute the underlying premise for integration of
care for oncology fellows.148 palliative care and oncology. Thus, this knowledge must
The heterogeneity in education programmes (ie, the be compulsory in all curricula from undergraduate to
competence defined as needed in palliative care) probably postgraduate and specialist education programmes.
mirrors the heterogeneity in organisation and in what is In a 2016 study exploring attitudes and beliefs among
delivered in clinical palliative care across, and maybe oncology trainees regarding palliative care, 67% believed a
even within, countries. The present recommendations mandatory palliative care rotation was important; those
have similarities, but perhaps what is more striking is who had completed palliative care rotations were more
the broad scope introduced by the variation in aware of the role of palliative care services than those who
programmes across countries. had not done so (96% vs 74%).533 A survey of Canadian
oncologists found that oncologists were more likely to refer
Educational barriers to, and facilitators of, integration to tertiary palliative care services when they had completed
of palliative care and oncology a rotation in palliative care.164 Thus, being part of a larger,
Lack of education and training, and the common multidisciplinary team alongside palliative care colleagues
perception of palliative care as being end-of-life care allows oncologists to share the burden of complex care
only, have been identified in different settings.148,503,504,527,528 delivery, potentially also preventing burnout and com
A 2016 review, stated that education (in addition to passion fatigue.163 Oncologists’ willingness to engage with
policy and implementation) is a key barrier to palliative palliative care services correlates positively with self-
care integration in the USA.527 The education barrier reported comfort around managing end-of-life issues.174
is both of quantitative and qualitative nature. The The integration of oncology and palliative care should
quantitative aspect includes the insufficient numbers be a two-way street. A clinical rotation is essential for
of health-care workers with adequate training and integration of these disciplines, because it could help
education to provide oncology fellows to acquire knowledge of the basic
palliative care at their level in the health-care system, principles of symptom management and communication,
which is not confined to US settings. The qualitative understand when referral is appropriate, and build a
aspect includes the large variations in content across working and research relationship with the palliative care
countries regarding both undergraduate and post team. A rotation could also help to destigmatise palliative
graduate education and training. care, and might result in increased interest among

oncologists for subspecialisation in palliative oncology. absence of recognition of the added value of including
The latter subspecialisation could enhance recruitment palliative care in the standard treatment lines, financial
to an emerging discipline. Because many palliative care issues, difference in scope, or difference in focus (ie, the
specialists have a background other than oncology, tumour versus the host) between oncology and palliative
clinical rotation the other way round (ie, to oncology) is medicine. In line with others,315 we think a shift of the
also warranted. Similar to the way in which patient care paradigm towards models based on patient-centred care
might be improved by education of oncologists in is highly warranted at all levels, and education
palliative care, rotations in medical and radiation programmes should reflect this shift. Patient-centred care
oncology could be of benefit for palliative care fellows, to does not exclude targeting the tumour, but instead uses a
increase their familiarity with the natural history of combined approach—the tumour and the host. This
cancer, cancer treatment modalities, and the complex combined approach is a focus that needs to be taught. In
decision-making process surrounding cancer treatment our view, the strive to include the patient in education and
at the end of life. Such rotations might also help palliative practice is a general challenge of contemporary medicine.
care specialists and oncologists nurture a mutual Models such as shared decision-making are available, but
understanding, strengthen their partnerships, develop these are still strangers to most medical curricula.
common clinical pathways for their patients, and Communication skills are essential to provide patient-
enhance research collaboration. centred care. For patients with advanced cancer, the
To ensure and justify the investments in the integration patient-centred approach is of pivotal importance to ensure
of oncology and palliative care, the effectiveness of best possible care, whether oncological or palliative.
different teaching methods in palliative care education Training and education to improve physician-patient
and the benefits of single-profession and multiprofession communication as part of patient-centred education
education should be studied. The effect of how education programmes should, therefore, be emphasised in curricula
and training programmes on treatment, patient care, across different specialisations. Communication must be
and organisational issues (eg, care, economy, and learnt; thus, it must be taught as part of all curricula in
collaboration) needs to be documented, and the delivery basic, intermediate, and specialist medical education.
and effects of undergraduate and postgraduate education Oncologists and palliative care specialists should receive
on the promotion of palliative care integration mapped. specific communication training regularly to maintain and
Health-care organisations increasingly require evidence develop their skills, and to share fundamental skills.326,403
of the effect of education, so a robust evidence base to Several methods are available for teaching communication
justify the cost and time of delivering education in to clinicians; communication skills training with role play
palliative care must be established. and feedback, e-learning, group discussions, modelling,
Tertiary palliative care specialists are often located in case evaluations, and coaching are some of the most
comprehensive cancer centres or university hospitals, and commonly used strategies. Overall, strategies that are
are also commonly engaged in academic activities. active and involve practice seem to be most efficient.406
Leveraging of the skill-set of tertiary palliative care Recommendations are presented in panel 17.
specialists to support primary and secondary providers of
palliative care, and expansion of the scope of tertiary
palliative care beyond the cancer centre setting, through Panel 17: The role of education—recommendations
education and mentorship programmes, might help to • Ensure palliative medicine is accredited as a specialty or subspecialty in all countries
upskill primary and secondary providers and clarify the by encouraging public awareness of the needs and national and international
respective roles of each. Tertiary palliative care specialists recommendations of accreditation, and adapting the accreditation from successful
working in comprehensive cancer centres or in close countries
conjunction with oncological departments must have • Ensure mandatory teaching of palliative care subjects in medical, radiation, clinical
skills and competence in oncology. Although the level of and surgical oncology specialisation programmes
skill needed by these specialists has not yet been made • Develop a set of minimum volume and content requirements for use in these
concrete, they should have the skills and knowledge to programmes, including mandatory clinical rotation in palliative care
handle oncological emergencies, prognosticate different • Develop international teaching programmes on when and how to integrate
cancer diseases, and about chemotherapy and radiation oncology and palliative care by requiring programme development at the level of the
therapy to enable them to cooperate with the oncologist in health-care provider and from professional organisations (eg, European Society for
deciding the optimal treatment proposal for each patient. Medical Oncology, European Association for Palliative Care, European Society for
Education programmes in palliative medicine are Radiotherapy and Oncology, American Society for Radiation Oncology, and American
highly heterogeneous at all levels of health care, and Society of Clinical Oncology), and applying indicators for programme development
across countries and perhaps also within regions. This and implementation
heterogeneity is, in itself, a substantial barrier for further • Encourage continuous education of multidisciplinary teams in early integration and
integration of oncology and palliative care. One might in teamwork by requiring education for oncologists and palliative medicine
speculate whether this heterogeneity is related to the specialists in patient-centred care and early integration
immaturity of palliative care as a medical specialty, the

Research journey—from the time of diagnosis of advanced cancer.

With increasing integration of oncology and palliative Patients are often concurrently managed by the oncology
care, specialist palliative care is no longer only involved in and palliative care teams, creating ample opportunities
the last days and weeks of life, but throughout the disease for collaborative research to improve patient care.
A 2011 systematic review16 that examined the quantity,
Opportunities Challenges design, and scope of palliative oncology publications,
1 Sharing of clinical and research expertise Need time to communicate and build the identified significant gaps in the literature. Of 1213 articles
trust and relationship between teams included over two 6-month periods, 365 (30%) were reviews
2 Access to patients (eg, enrolling patients from oncology Potential conflicts between teams or systematic reviews. More than half of the studies (n=438,
clinic to assess palliative care needs) because of differences in approaches 52%) focused on physical symptoms among patients with
3 Opportunities for new areas of research and discoveries at Potential competition for study cancer, with few studies examining the interface between
the interface of disciplines (eg, defining roles and leadership
responsibilities for delivery of palliative care by oncologists) oncology and palliative care, and how palliative care can be
4 Sharing of work (eg, expertise) and resources (eg, staffing) More resources might be needed to better integrated with oncology to improve care. Patients
might reduce overall cost allow larger research teams with more than 6 months, 4–6 months, and less than
3 months to live each constituted approximately one-third
Table 8: Opportunities and challenges for integrating oncology and palliative care teams to do research
of studies; however, patients with longer survival
(>12 months) and very short survival (<1 month) were
Panel 18: Research opportunities related to integration of palliative care and under-represented.534 Only 6% of studies were randomised
oncology—recommendations of future research questions controlled trials, with low-quality reporting.136 Thus,
substantial opportunities to improve both the quantity and
Specialist palliative care referral quality of palliative oncology studies remain.
• What is the optimal timing for palliative care referral (eg, resource-rich vs In this section, we will focus our discussion on
resource-poor settings, large vs community hospitals, and cancer vs non-cancer)? three major areas of research parallel to increased
• Should time-based or need-based criteria be driving palliative care referral? integration between oncology and palliative care: system-
• Can standardised referral criteria coupled with automatic referral streamline the oriented health services studies to examine different
referral process? models of care, and understand the optimal processes and
• What strategies can help to overcome barriers to referral among patients and outcomes of improved integration of oncology and
oncologists? palliative care; patient-centred research to examine physical
• What is the effect of palliative care intervention on patients’ ability to complete cancer symptoms, psychosocial distress, communi cation, and
treatments? decision-making preferences throughout the disease
• What is the role of palliative care for patients with curable cancer? trajectory; and public health-oriented research to examine
Palliative care programmes external validity of the integration of palliative care and
• What is the standard (minimum requirement) for a palliative care programme in oncology in the whole society (eg, a region or a country),
different health-care settings? and to develop and evaluate societal implementation
• What are the advantages and disadvantages of various novel models (eg, palliative strategies. Some of the opportunities and challenges to
care teams involved in multidisciplinary tumour boards or embedded clinics)? integration of palliative care and oncology that would
• What should be the metrics or benchmarks to measure the success of a hospital, benefit from research attention are highlighted in table 8.
region, or nation on palliative care delivery?
• How can a clinical practice guideline on palliative care be developed and used to Opportunities for system-oriented research
inform practice? A growing number of studies have addressed potential
• How can primary care teams integrate to provide palliative care? benefits of early integration of palliative care in
oncology.3,5,47–51 The question is no longer whether patients
Education would benefit from palliative care, but how palliative care
• How much palliative care do oncologists need to know to deliver effective palliative oncology teams need to provide care, when is the optimal
care? timing for referral to specialist palliative care, how
• How much oncology do palliative care specialists need to know to deliver effective comprehensive do the palliative care teams need to be,
care? and what is the minimum model for care delivery. A 2016
• What are the most effective strategies to educate oncologists about palliative care? Delphi study471 identified 11 major criteria to refer patients
• How can the training and accreditation for specialist palliative care be standardised in with advanced cancer to outpatient palliative care. Some
different countries? of the main questions regarding system-oriented research
Public policy in palliative care are summarised in panel 18.
• What public policies are most effective to drive palliative care? A 2015 systematic review52 highlighted 38 aspects
• What are some strategies that professional organisations can adopt to support of integration under five main domains: clinical
integration? structures, clinical processes, administration, education,
• How can investment in palliative care programmes be optimised to maximise the and research. Although many ideas exist on how inte
value of health-care expenditure? gration can take place, empirical data are lacking to show
improved outcomes outside of a clinical trial. Few studies

have examined how routine symptom screening coupled Patients with chronic progressive diseases, including
with care pathways can be used to refer patients to cancer, frequently receive care in multiple settings,
palliative care.348,535 Moreover, there is tremendous including their home, acute care hospitals, palliative care
opportunity for joint research studies between oncology units, inpatient hospices, and long-term care facilities.35
and palliative care teams to investigate the process of The monitoring and screening of patient-reported and
collaboration between the oncology and palliative care caregiver-reported outcomes needs to accompany the
teams, such as multidisciplinary teams and embedded patient to those multiple settings. The Edmonton
palliative care clinics.536 Regional Palliative Care Program did some pioneer
Resource limitations mean specialist palliative care for research on adoption in multiple areas of care,544–546 which
every patient is not possible. A proportion of patients was followed by several international initiatives.547,548 More
with low levels of distress could be managed by their research is needed to define the best ways to provide
oncology team. In some countries, primary care also valuable information to clinicians throughout the
plays an important role as front-line provider. How much trajectory of patient care in multiple settings and clinical
palliative care do oncology teams and primary care circumstances. Possible research opportunities in the
providers need to know521 and deliver in their daily area of screening and monitoring of patients with cancer
practice?469 In a survey174 of oncologists, greater knowledge and their caregivers are summarised in panel 19.
and comfort with palliative care was associated with Palliative care and oncology teams need to work
higher levels of self-reported palliative care delivery and together to develop and validate novel assessment tools
specialist palliative care referral. Oncologists and on various patient-reported outcomes, and apply these
palliative care teams can collaborate to examine how to instruments in clinical and research settings to assess
better integrate palliative care competencies in oncology health outcomes. The patient-reported outcomes
and primary care, and to document the patient care measurement information system has developed
outcomes associated with this integration. multiple assessments on the basis of computer adaptive
Another area of development in system-oriented testing, but these assessments require further testing.549
research is the assessment of the level of integration In 2017, the International Consortium for Health
among cancer centres. Such a metric would allow Outcomes Measurement recommended a standard set of
patients and clinicians to identify institutions that offer a patient-centred outcomes for patients with colorectal and
high level of palliative care, researchers to examine breast malignancies.550,551 Assessment of personalised
progress, and administrators and policy makers to triage symptom goals might allow both oncologists and
resources and develop quality improvement initiatives. palliative care teams to determine the individual response
A 2015 international Delphi study,44 identified a high level to symptom interventions and further tailor treatments.552
of consensus for 13 indicators under four domains
(clinical structure, process, outcomes, and education).
Further studies are needed to validate this set of criteria. Panel 19: Research opportunities related to symptom assessments—research
recommendations
Symptom assessment
There is considerable evidence that patients with advanced Symptoms and needs screening
cancer develop multiple devastating physical and • Which validated assessments should be used for which domains for screening in
psychosocial problems,537–539 and that these problems place various clinical settings (eg, oncology, palliative care vs other specialties, or inpatient
substantial burden on their primary caregivers.540,541 vs outpatient)?
Frequent monitoring of these clinical problems will allow • What instruments or assessments should be included in a standardised
oncologists and palliative care specialists to identify comprehensive palliative care assessment?
patients who would benefit from various pharmacological • How can patient function be assessed accurately?
and non-pharmacological interventions (see the back • How can screening be best conducted for concepts such as patient understanding of
ground section of this Commission and the section on illness, communication styles, spirituality, and caregiver needs?
prognostication). More systematic prospective monitoring • How can patient, health-care professional, and system barriers be overcome to
of symptoms might contribute to better prognostic facilitate routine screening in a busy oncology and palliative care practice?
models, which is warranted (see the section in this • How can electronic data capture be used to collect and display patient-reported
Commission on prognostication); however, the adoption outcomes?
of regular monitoring of patient-reported outcomes has • What strategies can professional organisations adopt to support integration?
been erratic. This inconsistency is partly because of the • How can investment in palliative care programmes be optimised to maximise the
absence of standardisation or consensus on which value of health-care expenditure?
domains require monitoring, the limited degree of Assessment of treatment response
validation of some instruments, the barriers to • What is the minimum clinical important difference and responsiveness to change for
implementation of routine screening, and the need for various scales? How can personalised symptom goals be used to augment practice?
more research to ascertain the real effect of screening on • What are the predictors of treatment response?
patient outcomes.542,543

improve the detection and treatment of pain by

Panel 20: Research opportunities related to symptom management—research oncologists, palliative care specialists, pain medicine
recommendations specialists, and other professions.
Treatment toxicities Although specialist palliative care has been found to
• How can adverse effects in clinical trials and daily practice be better assessed? improve symptom control compared with oncology care
• What is the pathophysiology of adverse effects related to novel therapies? alone,63 many symptoms have few effective therapies and
• What are novel supportive care interventions for various treatment-related adverse remain undertreated even by a comprehensive palliative
events? care team552,560—eg, anorexia-cachexia is reported in up
to 60% of patients with advanced cancer. Management of
Cancer-related symptoms cachexia should begin at the precachexia phase, when
• What is the pathophysiology, and what are the potential therapeutic targets? patients are seen predominantly by their oncologists.
• What combination of multimodal therapy has the greatest effect on symptom outcomes? Here, multimodal multidisciplinary interventions target
• What validated outcomes are required for regulatory approval for symptoms such as ing nutrition, physical activity, inflammation, appetite,
fatigue, cachexia, and dyspnoea? and nutritional impact symptoms are essential.561,562
• How to address chemical coping and opioid addiction in cancer patients while Collaborative research between oncologists and palliative
providing good pain control? care teams to develop evidence-based palliative inter
ventions can be fruitful (panel 20). By contrast, other
issues, such as delirium and signs of impending death,
Panel 21: Research opportunities related to psychosocial support, communication, mostly occur in the last days and weeks of life, and do not
and decision making—research recommendations require a high degree of collaboration.259,563,564
Psychosocial, spiritual, and caregiver care Psychosocial issues and communication

• What interventions are best for adjustment disorders? Palliative care teams can support oncology teams in the
• What are the strategies to screen for spiritual care needs in the medical setting? delivery of psychosocial support and patient and family
• What are the best interventions to support caregivers along the disease trajectory? communication.50,307,357 There is a great opportunity for
• What are the strategies to support decision making? research on the best methods for the delivery of effective
• How can bereaved caregivers at risk of complicated grief be supported? psychosocial support, and on methods of communication
Communication and decision making with patients and their families. Randomised controlled
• How can survival in advanced diseases be accurately predicted, and used to support trials can be done on physician body posture,565,566
decision making? discussions regarding resuscitation,567 and the effect of
• What are the strategies to communicate prognosis and help patients gain a better the content of the physician’s message.470 Better prog
understanding of their illnesses without jeopardising the patient–clinician relationship? nostication and prompt sheets might also enhance
• How can serious illness conversations be facilitated over the continuum of disease? communication.277,408,568,569 Important areas of psychosocial
• How can decision-making aids and prompt sheets be standardised? support, communication, and advance care planning in
• How can physicians tailor the decision-making process to different decision making which palliative care teams can develop research
preferences among patients and families? initiatives together with oncology teams are summarised
in panel 21.
Symptom management Public health and implementation effect

Multiple factors contribute to physical and psychosocial The clinical and social contexts of death and dying in
distress, including cancer location and burden, toxicities cancer are changing rapidly. Globally, WHO strongly
of cancer treatment, and comorbidities. As cancer supports advocacy efforts to make essential medicines
treatment evolves, new treatments, such as targeted and available for palliative care. This public health policy
immune therapies, have dramatically modified the risk- work is grounded in the theory that, at a national level,
to-benefit ratio, adding another layer of complexity to palliative care programmes need to be context dependent
cancer treatment decisions at the end of life.181,553–555 and implementable. Place of death, place of care at the
Oncology teams are experts in the use of many of these end of life, access to palliative care, circumstances of
new modalities, and palliative care teams are experts in dying, and end-of-life decisions are strongly related to the
symptom evaluation and management. health-care system, legal context, and type and models of
Many symptoms, such as fatigue, pain, anorexia, and palliative care available within a country. Therefore, more
dyspnoea, are highly prevalent throughout the disease implementation research is needed regarding integration
trajectory.556,557 In a systematic review and meta-analysis of palliative care and oncology.
of 52 studies covering 40 years,558 cancer pain was present Most evidence on integration of palliative care and
in more than 50% of patients, and with one-third of oncology is based on clinical or health service evaluation
patients reporting moderate or severe intensity, which studies done in only one or few hospitals.3,5,47,50,58 In most
was confirmed in a subsequent meta-analysis.559 This countries, how well integration of early palliative care
high prevalence calls for more research and resources to and oncology has been implemented throughout the

health-care system is, as yet, unknown. Palliative care is and the broader community in early palliative care, more
increasingly recommended in patients with cancer, but public health-oriented research is needed alongside
seldom offered to all in need. In an observational study570 clinical and health services research. Important domains,
of 4466 deaths in four European countries, palliative care possible research methods for monitoring the imple
was shown to be delivered to 50% of patients in Belgium, mentation of integration across a country, and possible
55% in Italy, 62% in the Netherlands, and 65% in Spain. research aims for public health studies relevant to inte
Palliative care specialists attended to 29% of patients in gration of palliative care and oncology, are summarised in
the Netherlands, 39% in Italy, 45% in Spain, and 47% in panel 22.
Belgium. In this international study, patients with cancer
were twice as likely to receive palliative care than patients What are the opportunities for collaborative research
with non-curable diseases. Furthermore, if palliative care regarding cancer treatments?
is delivered, it is often initiated at the very end of life for Palliative care teams are increasingly involved in the care
most patients, when the patient is a few weeks before of patients undergoing palliative therapies for advanced
death. A nationwide study571 in Belgium showed that the cancer, including systemic therapies, radiation, and
time of onset of palliative care is a median of 20 days surgical procedures. These teams have a crucial role in
before death for patients with cancer, as compared with helping to maximise the quality of life of patients receiving
12 days in heart failure and 10 days in COPD. cancer treatments, and also in facilitating the complex
Hence, this Commission shows that most patients decision-making process surrounding treatments at the
do not receive palliative care early in their disease end of life (ie, the last months before death). The advent of
trajectories. Furthermore, the level of specialised care novel therapies, such as immunotherapies, creates even
delivered to patients with advanced cancer in university more opportunities for collaborative research between the
hospitals often is quite different from the care in other oncology and palliative care teams to optimise patient
settings. As the majority of the palliative care trials have outcomes.
been done in university hospitals, research findings are Exciting opportunities exist for joint research, through
not necessarily applicable to other settings.572 collaborative efforts by these two groups, which could
lead to a better understanding of the pathophysiology
New public health studies of treatment-related adverse effects. The interaction
New public health approaches present a new research between cancer burden, treatment toxicity, and comor
perspective, using evidence from health promotion, bidities is complex and variable. As an example, a highly
health behaviour, and public awareness building.573,574 effective immunotherapy will reduce symptoms related to
Patients with cancer are cared for by oncologists or
physicians for only a small amount of time—it is the
spouses, families, and broader community that care for Panel 22: Research opportunities related to public and population health
these people full time. Hence, the effect of family,
Recommendations of research methods
volunteers, and the larger community is extremely
Monitoring implementation scope
important for patients with cancer; they support not only
• Administrative databases
the patient’s wellbeing, but also in the expression of their
• Health-care registries, eg, nationwide sentinel networks
care preferences, participation in SDM, and eventually in
• Nationwide post-mortem surveys
the decisions at the end of life.
• Auditing of integrated care services
From this perspective, one should bear in mind that
the general public, and thus public opinion, might not Recommendations of research aims
yet fully understand the potential of integration of early Evaluate the quality of integration of palliative care and oncology
palliative care in an oncology treatment trajectory. The • Development of palliative care quality indicators for the evaluation of the quality of
reality, in most countries, is that palliative care is still the integrated services
very much taboo or is associated with stigma because • Cross-country and cross-setting (university hospital vs local hospital) validation of the
awareness and experiences of palliative care potential are indicators
limited to terminal care; hence, palliative care is • Implementation of the quality indicators
associated with imminent death. To address this • Development of quality improvement interventions
problem, we need research into the development of Implement health-promoting early palliative care in cancer
palliative care public awareness campaigns, human • Assessment of the perceptions of palliative care potentials among cancer patients and
behaviour in health crisis situations, and empowerment their families, health-care professionals, and the general public
of patients and families in making the right decisions • Development of health promotion campaigns to empower cancer patients and their
both for their cancer treatment and for their wellbeing families to talk to their health professionals early in their illness trajectory about
and quality of life. palliative care needs and care preferences
To increase the amount of evidence concerning • Development of palliative care awareness campaigns to improve knowledge and
implementation of early palliative care in oncology and attitudes towards early palliative care in cancer patients and the general public
improvement of the involvement of patients, families,

the tumour mass and also improve the patient’s and Evolving models to support collaborative research
caregiver’s psychological wellbeing, but will add symptoms Compared with established medical disciplines, such as
related to fatigue and immune-related adverse effects, such oncology, which focus on management of specific
as dermatitis, colitis, and hypophysitis.575 Cancer, either diseases, palliative care focuses on personhood care.
through its direct effect on organs and tissues or its indirect Thus, palliative care specialists are uniquely positioned
effect on systemic mediators, can result in multiple to do research by drawing on the similarities among
symptoms, decreasing patients’ functioning and quality of different diseases to derive common principles of patient-
life. Cancer treatments might control tumour growth, but centred care (eg, management of dyspnoea and serious
might also lead to significant toxicities. Comorbidities illness conversations), while personalising management
could further contribute to the overall symptom burden. based on the unique differences among the different
Supportive care and palliative care aim to alleviate diseases (eg, cancer trajectory is more predictable).
symptoms and improve quality of life by modulating the Although there is no scarcity of academic oncologists,
afferent signals and enhancing the coping mechanisms. palliative care researchers are in short supply. Thus,
Palliative care specialists need not only to collaborate educational programmes and funding opportunities are
with surgeons, radiation oncologists, medical oncologists, needed to train more palliative care clinicians in the
and haematologists clinically, but also to conduct principles of research and unique aspects of doing
research studies to identify the best ways to optimise palliative care studies. Such investments will probably
patients’ functional status and nutritional status before, result in more opportunities for research collaborations,
during, and after treatments. More research is also and will accelerate development of innovative inter
needed to determine the best strategies to prevent or ventions to improve patient care.
treat various treatment-related adverse events. As new therapies become available to patients with
Cancer treatments close to death are associated with cancer, opportunities will arise for oncology and palliative
reduced quality of end-of-life care.576,577 Novel targeted care teams to prepare proposals aimed at carefully
therapies and immunotherapies are generally associated measuring the effect of those therapies in the physical
with fewer side-effects than conventional chemotherapy, and psychosocial wellbeing of the patients, and the
and are increasingly offered to patients with reduced ideal management of the symptomatic complications
performance status.555 A small proportion of these secondary to those therapies. These proposals will
patients experience a remarkable treatment response, provide access to sources of funding from industry,
altering the natural history in a significant manner and which traditionally have been largely unavailable to
adding to the prognostic uncertainty. Whereas oncologists palliative care research teams. At a time when academic
can offer hope through new treatment opportunities, funding is becoming less available, these joint efforts will
palliative care teams can nurture hope for better quality of provide support for logistics and career development of
life throughout the disease trajectory and help patients to academic palliative care physicians and oncologists.
balance the ever-shifting priorities. More collaborative
research is needed to better understand patients’ goals of Conclusion
care, illness understanding, and treatment preferences to Many questions related to the optimal delivery of
develop better prognostication tools and decision aids to palliative care in patients with cancer remain
inform the complex decision-making process regarding unanswered, with many challenges to high-quality
treatment continuation and discontinuation as death research. With increased integration between oncology
approaches.181,299 and palliative care, tremendous opportunities exist to
identify novel research questions at the interface of
disciplines, combine the resources to complete high
Panel 23: Research—recommendations quality research, generate new knowledge to advance
• Encourage research into new public health approaches for integration of oncology symptom management and care delivery, and develop
and palliative care by establishing international and national research programmes to better models of integrated care to improve patient
support research on content, methods, and how to verify the effects outcomes. Recommendations are presented in panel 23.
• Develop a minimum and maximum set of indicators for the follow-up of successes in
the implementation of early integration of oncology and palliative care by initiating Summary and call for action
research programmes internationally and nationally During the preparation of this Commission, the hetero
• Initiate collaborative research programmes in oncology and palliative care for symptom geneity of the organisations, the content of the models,
management (needs) and their application in secondary palliative care and in the and the performance in clinical practices have become
discussion in multidisciplinary teams by initiating research programmes internationally evident. The heterogeneity goes even further into the
and nationally content of the education programmes, including the
• Ensure top academic positions in palliative medicine or care (professors) are present at presence of palliative care in oncology training (if present
all academic cancer centres and medical schools by initiating professional awareness at all), and the structure, content, and (absence of)
programmes and advocacy groups formalisation of palliative medicine as a specialty in
many countries. This heterogeneity together with the

absence of international agreements and standards of and the health-care bureaucrats need to develop plans
palliative care in oncology is probably the main barrier to and implementation strategies, and combine these plans
successful integration. If one of the partners in a with economic incentives and basic funding of the inte
relationship is undefined or ambiguous, the probability gration between oncology and palliative care. Palliative
to build a long lasting relationship will probably be low care might reduce costs, and improve the quality of life of
and very challenging. patients and that of their family members.
Policy Cultures
Internationally, strong and clear resolutions and recom Cultures in health care play important roles by serving as
mendations are given by WHO, OECD, professional invisible roadmaps for interpersonal interactions—eg,
organisations (ASCO, ESMO, EAPC), and international how a doctor communicates with a patient, or how
charters (EAPC, IAHPC, WPCA) on the place of palliative physicians with different specialties interact. Cultures
care as a part of cancer care programmes. The content also act as barriers to the process of changing and
and directions can be summarised by the statement given improving practice. The oncology culture can be described
by the World Health Assembly: “Palliative care as an as a tumour-directed culture, with its positive implication
essential component of comprehensive care throughout when the treatment goal is to cure and thereby achieve
the life course”.578 This states that palliative health services tumour control and, ideally, total eradication of the
for non-communicable diseases should be covered under tumour. This culture has been, and is, essential to
national universal health coverage plans. Several high- improve cure for many cancer diagnosis. However, from
quality studies have shown that an integration of palliative a patient’s perspective, if cure is not achievable,
care into oncology care improves outcomes like symptom a combined tumour-directed and patient-centred
management, patients’ and family members’ quality of approach is needed, and strongly recommended in this
life, and possibly survival for patients with short life Commission. In palliative care culture, the primary focus
expectancy. Systematic use of PROMs improves symptom is to improve patients’ quality of life. In this Commission,
control, reduce psychological distress, and can improve patient-centred care, including SDM with a primary focus
survival. The need for integration is further supported by on the patient (the host) is recommended. The palliative
the increase in incidence and prevalence of patients living patient-centred culture therefore differs from the
with advanced cancer. oncology culture: it has different players and has, until
These clear and strong recommendations, which have recently, been organised separately from mainstream
arisen over the past couple of decades, are contrasted by health and oncology care in many countries. From the
the findings in this Commission: an absence of perspective of a patient in a non-curative situation, the
integration of oncology and palliative care. In most palliative culture needs to be present and should not be
national cancer care plans, palliative care is not
formulated as an integrated approach together with
oncology. If it is present, it is often an add-on to the Panel 24: Recommended national and international actions
tumour-directed approaches. It seems to be a lack of • True integration of oncology and palliative care must be recommended by national
willingness and capability to implement and prioritise health-care authorities, followed up with resource allocation and priorities, and
palliative care in the cancer care plans, in care monitoring of successful implementation. International valid indicators of successful
programmes, and in clinical care pathways. integration of oncology and palliative care are needed
The absence of true implementation might, in addition • Analysis of the medical cultures and implementation of palliative care on the basis of
to the aforementioned factors, be related to the the involvement of the leaders of the oncology and palliative care programmes are
heterogeneity of the organisational models of palliative needed. The unofficial leaders at all levels also need to be mapped and involved in
care, the absence of systematic education in palliative implementation plans
medicine in medical schools and during specialisation in • International standards of oncology and palliative care are needed for: Integrated
oncology, and the lack of education about oncology oncology and palliative care models to evaluate the effects of these models clinically;
during palliative medicine specialisation. palliative care education in oncology and oncology education in palliative medicine;
One might ask, has palliative care become even more and definition of the necessary competence and the content of the education at the
underprioritised? Over the past decade, much attention three different layers at a high level, preferably internationally, and not governed by
has been given to the advances of new systemic tumour- tradition or local preferences
directed therapies, and, at the same time, attention on • Patient-centred care must be actively implemented into oncology care by means of
patient-centred care might have dwindled. systematic use of standardised care pathway where oncology and palliative care is
To achieve improvements in complex systems like fully integrated. Patient-reported outcome measures and shared decision making are
health care, several approaches are needed, and a methods that should systematically and actively be used in all parts of cancer care
combination of top-down and bottom-up actions are • Investment in research is urgently needed to develop an evidence base on how to
required (panel 24). In this Commission, we recommend organise and perform palliative care in oncology practice. National earmarked grants
that the strong political recommendations are followed for research programmes are needed, which are sufficiently funded for 3–5 years.
up at national and regional levels. Together, politicians

considered to be in competition, but rather synergistic or during a disease trajectory. Many patients with cancer
integrated with the tumour-directed culture. undergo life-prolonging treatment for years, or are
One of several ways to understand why the patient- cancer survivors with manifest or latent late effects of
centred palliative care approach is not implemented into treatments. Therefore, the chronic disease model is
oncology clinics is the gap and antagonisms between the highly relevant in oncology, but is seldom referred to or
two cultures (panel 24). When different approaches from used.
two cultures are to be blended in cancer care programmes, Patients and their families expect, and demand, to be
one needs to understand the differences and shared actively involved in the care planning at all stages of the
values, and plan the implementation according to a disease trajectory. A central part of the involvement and
multicultural reality. The antagonisms held by the engagement of patients is a systematic collection of the
two maintain status-quo (ie, we vs them) is, in our view, a patients’ voice. Expectations exists about information
substantial barrier to integration. and communication to patients about treatment and care
plans, which often are not fulfilled when it comes to
Organisation and competence patients with advanced disease and a limited life
The overall aim of the organisational model is that expectancy. Often, they are not aware of their disease
patients and their families have access to the care they status, and the expected effects of tumour-directed
need, when they need it, resulting in improved health- treatment.
care outcomes. In the integrated oncology and palliative The fragmented nature of the cancer care system calls
care model, early integration is a key concept. This for a method to implement the planning and coordination,
concept illustrates that the content and competence of and to allocate resources according to patients’ needs. An
palliative care is much more than end-of-life care. SCP is a method to plan and implement complex health
The multidisciplinary team approach can be used as a services, and to ensure that the right people are at the
key component of the organisational model in hospitals right place at the right time. This Commission proposes
to link oncology and palliative care services. However, the the use of SCP as a model to develop a seamless patient
organisations need to do community and home care flow in a customised organisational model.
outreach. The models need to have a clear and robust Symptom assessment by systematic use of validated
organisation, but also be flexible according to the PROMs is pivotal for patient-centred care throughout the
patients’ needs. Several organisational models of whole cancer disease trajectory. Symptom assessment is
palliative care have been developed and evaluated. This a key method to engage patients in the decision-making
Commission recommends the models be divided into processes in which PROMs are key information to
three levels: primary, secondary, and tertiary care. This customise the SCPs. PROMs were traditionally collected
Commission also recommends that the place and via paper-based questionnaires. This Commission
competence of oncology and palliative care need to be recommends development and use of electronic tools for
adjusted to the level of care and the patients’ needs. At collection of e-PROMs that can be integrated into the
the primary health-care level, general practitioners need electronic patient record systems.
to have the necessary competence in palliative care. Their SDM is another central component of patient-centred
role is central in home care. care. It is highly relevant in all phases of cancer treatment,
One limitation of the organisational models identified but is even more central for patients with advanced non-
in the literature and discussed in this Commission is curable disease. SDM is an active and continuous process,
their heterogeneity, which hinders the generalisation of combining the tumour-directed and patient-centred
findings. This Commission has identified a need to approaches in the care planning. This Commission
develop international standards for the structure and recommends SDM is included as a mandatory part of
content of the organisational models, and to further oncology guidelines, and is visualised in the content of
evaluate the effects in public health-care research. the SCPs (panel 24).
For the successful integration of oncology and palliative
care, a multidisciplinary approach is needed (panel 24). Research
The health-care providers need skills in patient-centred Early integration of oncology and palliative care gives new
care. Wide variations in education have been identified arenas and opportunities for collaboration to address new
for oncologists and palliative medicine specialists, and research questions. Some key questions to answer are
variations also exist for education of the other participants related to health-service issues and others to patient-related
in the multidisciplinary teams. The general lack of issues, such as assessment and treatment of physical
competence in palliative care is also a barrier to successful symptoms, psychological distress, communication, and
implementation of the integrated models. decision-making processes and performances.
New tumour-directed treatments, such as targeted and
Patient-centred care immune therapy, have added another layer to the
The concept of total pain, which is central in palliative complexity of the end of life. These treatments give new
care, infers a broad understanding of patients’ needs opportunities for collaborative research in addressing the

interactions between tumour burden, treatment toxicity, 7 Ferris FD, Bruera E, Cherny N, et al. Palliative cancer care a
and comorbidities. At the health-service arena, several decade later: accomplishments, the need, next steps—from the
American Society of Clinical Oncology. J Clin Oncol 2009;
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oncology and palliative care be optimised? What are the 8 WHO. Technical brief no 1. Integrated health services–what and
optimal organisational models at the primary, secondary, why? World Health Organization, 2008.
9 Taylor C, Munro AJ, Glynne-Jones R, et al. Multidisciplinary team
and tertiary levels of care for integrated oncology and working in cancer: what is the evidence? BMJ 2010; 340: c951.
palliative care? How can the human resources be used 10 Choi BC, Pak AW. Multidisciplinarity, interdisciplinarity and
optimally in the SCPs? transdisciplinarity in health research, services, education and policy:
1. Definitions, objectives, and evidence of effectiveness.
Research competence and funding are basic (panel 24). Clin Invest Med 2006; 29: 351–64.
Few resources are allocated to palliative and end-of-life 11 Tangka FK, Trogdon JG, Richardson LC, Howard D, Sabatino SA,
care research. Data from several countries indicate that Finkelstein EA. Cancer treatment cost in the United States: has the
0·3–1% of resources allocated to cancer research go to burden shifted over time? Cancer 2010; 116: 3477–84.
12 Cancer trends progress report–2011/2012 update. US National
cancer palliative care research. Insufficient research Institutes of Health, 2012.
funding also minimises the opportunities for training 13 Mariotto AB, Yabroff KR, Shao Y, Feuer EJ, Brown ML. Projections
physicians in palliative care research, and thereby qualify of the cost of cancer care in the United States: 2010–2020.
J Natl Cancer Inst 2011; 103: 117–28.
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positions. cost-saving effect is larger for cancer patients with higher numbers
Contributors of comorbidities. Health Aff 2016; 35: 44–53.
All coauthors participated in writing and editing of the Commission. 15 Ferrell BR, Temel JS, Temin S, et al. Integration of palliative care
Final writing and editing was done by SK, JHL, MJH, and TL. into standard oncology care: American Society of Clinical Oncology
clinical practice guideline update. J Clin Oncol 2017; 35: 96–112.
Declaration of interests 16 Hui D, Parsons HA, Damani S, et al. Quantity, design, and scope of
SK and JHL are Eir-solution stockholders. MA reports personal fees the palliative oncology literature. Oncologist 2011; 16: 694–703.
and non-financial support from the Multinational Association for 17 Kaasa S, Radbruch L. Palliative care research—priorities and the
Supportive Care in Cancer and the European Society of Medical way forward. Eur J Cancer 2008; 44: 1175–79.
Oncology; grants and personal fees from Helsinn and Sandoz; and 18 Usborne CM, Mullard AP. A review of systemic anticancer therapy
personal fees from Tesaro, Merck USA, VIfor, Pfizer, Taiho, Kyowa in disease palliation. Br Med Bull 2018; 125: 43–53.
Kirin, outside the submitted work. TA reports grants from the 19 Spencer K, Parrish R, Barton R, Henry A. Palliative radiotherapy.
European Commission and the Ministry of Health of Slovenia during BMJ 2018; 360: k821.
the study; and grants and personal fees from Pfizer Oncology outside 20 Heikkilä R, Kaasa S. Chemotherapy in end-of-life care. Ann Oncol
the submitted work. ACa reports grants and personal fees from 2017; 28: 684–85.
Italfarmaco; personal fees from Sandozand Pierre Fabre Institute; and 21 Peppercorn JM, Smith TJ, Helft PR, et al. American Society of
grants from Molteni, Gruenenthal, and Ipsen outside the submitted Clinical Oncology statement: toward individualized care for patients
work. MF reports grants from GW Pharmaceuticals during the study. with advanced cancer. J Clin Oncol 2011; 29: 755–60.
DH reports grants from Helsinn, Teva, and Insys outside the submitted 22 Schnipper LE, Smith TJ, Raghavan D, et al. American Society of
work. KJ reports personal fees from MSD, Helsinn, Tesaro, Amgen, Clinical Oncology identifies five key opportunities to improve care
Pfizer, Merck, and Hexal outside the submitted work. RP reports grants and reduce costs: the top five list for oncology. J Clin Oncol 2012;
from European Commission, Health Programme of the EU, CANCON 30: 1715–24.
project during the study. The other authors declare no competing 23 Kimmelman J. Is participation in cancer phase I trials really
interests. therapeutic? J Clin Oncol 2017; 35: 135–38.
24 Rochigneux P, Raoul JL, Beaussant Y, et al. Use of chemotherapy
Acknowledgments near the end of life: what factors matter? Ann Oncol 2017; 28: 809–17.
First we express our sincere gratitude to Cassandra Coburn for her 25 Shepherd HL, Tattersall MH, Butow PN. The context influences
inspiring and invaluable support throughout the work with this doctors’ support of shared decision-making in cancer care.
Commission. We also thank the Istituto Tumori, Milan, for hosting the Br J Cancer 2007; 97: 6–13.
kick-off meeting and Tit Albreht for having resources to support it. 26 Matsuyama R, Reddy S, Smith TJ. Why do patients choose
We thank Gitte Tvetenstrand Korman for invaluable practical support chemotherapy near the end of life? A review of the perspective of
throughout the project. We thank Nina Aass, Anne Kari Knudsen, and those facing death from cancer. J Clin Oncol 2006; 24: 3490–96.
Julian Hamfjord for sharing their expertise that improved the manuscript. 27 LeBlanc TW, Tulsky JA. Communication with the patient and
family. Hanks G, Cherny NI, Christakis NA, Kaasa S, eds. Oxford
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Lancet Oncology Commission

Integration of oncology and palliative care: a Lancet Oncology

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reached by the continuous provision of realistic patient-

communication skills among the oncologists and

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and represents a paradigm shift within health care.40 The

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Jordhøy et al Temel et al Zimmermann Bakitas et al Maltoni et al Temel et al Grønvold et al

Y=presence of component in trial. Table adapted from Hui and colleagues.44,52

Table 1: Components of integration from seven randomised trials

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identified need for high-quality palliative and end-of-life

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The ASCO recommendations123 for early referrals to

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Variables included in score Type of prognostic estimate

Table 3: Summary of characteristics of palliative prognostic tools

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Patient-centredness in palliative care and oncology

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of life is both extensive and expensive,24,257 although such

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life.398 Honesty is commonly believed to undermine

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consequences, when these doctors are faced with clinical

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personal levels: implementation of a patient-centred

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counterpoised with integrated care, in which palliative

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Panel 12: Essential elements of secondary palliative care in oncology practices

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Cancer Control aims to address this issue, identifying

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