SPECIAL ARTICLE

5 European Society for Medical Oncology (ESMO)position paper on supportive and palliative care

K. Jordan1*, M. Aapro2, S. Kaasa3,4,5, C. I. Ripamonti6, F. Scotte,7, F. Strasser8, A. Young9, E. Bruera10,10 J. Herrstedt11,12, D. Keefe13, B. Laird14,15, D. Walsh16, J. Y. Douillard17 & A. Cervantes18

1Department of Medicine V, Hematology, Oncology and Rheumatology, University of Heidelberg, Heidelberg, Germany; 2Cancer Center, Clinique de Genolier,Genolier, Switzerland; 3Department of Oncology, Oslo University Hospital, Oslo; 4University of Oslo, Oslo; 5European Palliative Care Research Centre (PRC) NTNU,Oslo, Norway; 6Supportive Care in Cancer Unit, Department of Onco-Haematology Fondazione IRCCS, Istituto Nazionale dei Tumori, Milano, Italy; 7MedicalOncology and Supportive Care Department, Foch Hospital, Suresnes, France; 8Oncological Palliative Medicine, Clinic for Medical Oncology and Hematology,

15 Departement Internal Medicine, Cantonal Hospital St.Gallen, St. Gallen, Switzerland; 9Warwick Clinical Trials Unit, University of Warwick, Coventry, UK; 10Departmentof Palliative, Rehabilitation and Integrative Medicine, The University of Texas, MD Anderson Cancer Center, Houston, USA; 11Department of Oncology, ZealandUniversity Hospital, Roskilde; 12Department of Oncology, University of Copenhagen, Copenhagen, Denmark; 13Department of Medicine, Faculty of Health Sciences,University of Adelaide, Adelaide, Australia; 14Edinburgh Cancer Research Centre, University of Edinburgh, Edinburgh; 15St Columba’s Hospice, Edinburgh, UK;16Academic Department of Palliative Medicine, Our Lady’s Hospice and Care Services, Dublin, Ireland; 17ESMO, Lugano, Switzerland; 18CIBERONC, Department of

20 Medical Oncology, Institute of Health Research INCLIVA, University of Valencia, Valencia, Spain

*Correspondence to: Prof. Karin Jordan, Department of Medicine V, Hematology, Oncology and Rheumatology, Universitatsklinikum Heidelberg, Im Neuenheimer Feld 410,69120 Heidelberg, Germany. Tel: þ49-6221-56-6435; E-mail: karin.jordan@med.uni-heidelberg.de

25 Oncology has come a long way in addressing patients’ quality of life, together with developing surgical, radio-oncological andmedical anticancer therapies. However, the multiple and varying needs of patients are still not being met adequately as part ofroutine cancer care. Supportive and palliative care interventions should be integrated, dynamic, personalised and based on bestevidence. They should start at the time of diagnosis and continue through to end-of-life or survivorship. ESMO is committed toexcellence in all aspects of oncological care during the continuum of the cancer experience. Following the 2003 ESMO stand on

30 supportive and palliative care (Cherny N, Catane R, Kosmidis P. ESMO takes a stand on supportive and palliative care. Ann Oncol2003; 14(9): 1335–1337), this position paper highlights the evolving and growing gap between the needs of cancer patients andthe actual provision of care. The concept of patient-centred cancer care is presented along with key requisites and areas forfurther work.

Key words: position paper, ESMO, supportive care, palliative care, patient-centred care, multidisciplinarity

35 Introduction

Based on GLOBOCAN estimates, about 14.1 million new cancer

cases and 8.2 million cancer-related deaths occurred in 2012

worldwide [1]. Due to the accelerated pace of progress in diag-

nostics and treatments, more patients are now cured or live lon-40 ger with metastatic disease.

Nevertheless, a cancer diagnosis, the disease itself and the

sequelae of anticancer treatment are major stress factors for

patients. Over the last decade clinicians have accepted that, while

survival and disease-free survival are both fundamental factors,45 overall quality of life (QoL) is also crucial for patients. The latter

evidenced by the increasing use of QoL as high-level end points in

clinical trials of anticancer therapies [2–4].

Depending on diagnosis, cancer patients will receive different

types and intensities of tumour-directed treatment (i.e. antineo-50plastic therapy, radiotherapy and/or surgery). Along with antitu-

mour treatment, most patients need help to prevent and alleviate

side-effects and toxicities, and to cope with the disease itself.

Furthermore—at any stage of the cancer pathway—physical, psy-

chological, social, existential and spiritual support and rehabilita-55tion, are often needed. For optimal management, patients must

be fully involved in the decision-making process.

Building on previous ESMO policy statements and guidelines,

and considering the unfulfilled needs of cancer patients [5], this

position paper advocates for patient-centred care (including sup-60portive and palliative care) to be integrated by a multidisciplinary

team (MDT) to anticancer treatment, from the time of diagnosis

VC The Author 2017. Published by Oxford University Press on behalf of the European Society for Medical Oncology.All rights reserved. For Permissions, please email: journals.permissions@oup.com.

Annals of Oncology 00: 1–8, 2017doi:10.1093/annonc/mdx757

and throughout the continuum of disease, including end-of-life

and survivorship care.

ESMO is committed to increasing awareness and education to

bring patient-centred care closer to all professionals, to improving5 collaboration between healthcare providers for the good of patients

and to promoting research, so that patient-centred interventions

are not only integrated, but also based on the best evidence.

This paper was prepared by parts of the ESMO Faculty Group

on Supportive Care and Palliative Care. A meeting coordinated10 by the ESMO Educational Committee was held in May 2017 to

discuss the content and structure of the paper. The draft went

through several rounds of review by the group and was approved

by both the group and the Educational Committee Chair.

Supportive and palliative care: all about the

15 patient

Clinicians have always intended to provide the best care for their

patients. However, health systems do not always enable this.

Consciously putting patients’ holistic needs at the centre of every-

thing is the cornerstone of supportive and palliative care. This20 position paper goes beyond the debate about the standard defini-

tions of supportive, palliative and end-of-life care. Much work

has already been done in this area [6–8].

Two widely accepted definitions are provided below as

examples.25 The Multinational Association of Supportive Care in Cancer

(MASCC) has proposed the following definition of supportive care:

‘Supportive care in cancer is the prevention and management of the

adverse effects of cancer and its treatment. This includes manage-

ment of physical and psychological symptoms and side-effects30 across the continuum of the cancer experience from diagnosis

through anticancer treatment to post-treatment care. Enhancing

rehabilitation, secondary cancer prevention, survivorship and end-

of-life care are integral to supportive care’ [9].

The World Health Organisation (WHO) has proposed the fol-35 lowing definition for palliative care: ‘Palliative care is an

approach that improves the QoL of patients (adults and children)

and their families who are facing problems associated with life-

threatening illness. It prevents and relieves suffering through the

early identification, correct assessment and treatment of pain and40 other problems, whether physical, psychosocial or spiritual.

Addressing suffering involves taking care of issues beyond physi-

cal symptoms. Palliative care uses a team approach to support

patients and their caregivers. This includes addressing practical

needs and providing bereavement counselling. It offers a support45 system to help patients live as actively as possible until death’ [7].

While definitions are important and studies have shown that

the word ‘palliative’ may have negative connotations for patients

and could even delay their referral or readiness to accept inter-

ventions (when there is a lack of education or awareness of what50 supportive and palliative care entails) [10], efforts must be

focused on alleviating patients’ physical symptoms and psycho-

logical concerns, rather than on debating definitions.

The ESMO Supportive and Palliative Care Faculty proposes the

use of the term ‘patient-centred care’ [11, 12] to encompass both55 supportive and palliative care. To offer optimal patient-centred

care, institutions should be organised (according to their structure

and goals) in a way to make this possible, with the necessary level

of professional competence, skills and a collaborative organisation

that facilitates care pathways, individualised according to the needs60of each patient.

The patient-centred care approach

Individual cancer patients will express different physical, psycho-

logical, social, existential and spiritual needs at different stages of

the disease that will often evolve over time. Therefore, patient-65centred care cannot be standardised, even though it is provided

through a standard framework. To ensure that patients can voice

their needs, oncologists should incorporate detailed and routine

physical and psychological assessments allowing for supportive

and palliative interventions to be personalised and integrated in70the continuum of care. Patient-reported outcomes (PROs)

should be highly encouraged as requesting them has shown to be

associated with better QoL, fewer hospitalisations and even

increased survival compared with usual care [13].

Patient-centred interventions should be routinely discussed75and evaluated by the MDT, together with tumour directed treat-

ment, respecting patient preferences and cultural specificities.

Key patient-centred care interventions

The MDT caring for patients should be able to address their mul-

tiple and varying needs. Table 1 shows some examples of key80patient-centred care interventions regarding assessment, moni-

toring and management strategies.

Timely patient-centred interventions

Patient-centred care should be offered during the continuum of

illness, from the time of cancer diagnosis through to survivorship85or end-of-life. Needs will evolve together with the disease and

anticancer treatment, so ongoing and careful holistic evaluation

of requirements should be part of every consultation (see section

on key interventions above).

For some patients diagnosed at an early stage, the treatment90period is relatively short and, after follow-up, they become long-

term survivors or are considered cured (Figure 1, the curative

phase and survivorship phase). For these patients, rehabilitation,

prevention and management of adverse side-effects are most

important. Some patients will have one or more comorbidities at95the time of their cancer diagnosis that may require intervention

before the start of treatment; others may need rehabilitation due

to treatment-induced long-term adverse effects. When cancer

patients have advanced disease at the time of diagnosis, cure is

usually not possible (Figure 1, palliative phase and end-of-life100phase) and palliative care should be considered from diagnosis

onwards [14].

Recent studies show variable effects of the integration of early

supportive/palliative care interventions. A few systematic reviews

concluded that early palliative care in patients with advanced can-105cer significantly [15] or slightly [16, 17] improved patients’ QoL

and could decrease symptom intensity, although overall survival

was not prolonged. The most recent studies were not included in

Special Article Annals of Oncology

2 | Jordan et al.

these reviews. These results include negative studies [18]. The

overall impression is that early integration of palliative care

is beneficial to patients with advanced cancer at the time of

diagnosis [19].

5 Recently, dedicated outpatient supportive care teams focusing

on prevention and management of anticancer treatment toxicities

have been developed [20, 21]. Data from Italian [22] and French

[23] dedicated supportive care units show a reduction

of unplanned hospitalisations of cancer patients undergoing treat-

10ment [24] and for those requiring blood transfusion [25], allowing

for cost-effective management of symptoms and anticancer

treatment-related toxicity in an ambulatory setting [26]. However,

current literature is still scarce on supportive care units, so more

randomised clinical trial (RCTs) should be encouraged in this field.

15Survivorship, pre- and rehabilitation

Although patient-centred care is needed throughout the disease,

some phases deserve specific attention and more research. For

example, due to the improvement of anticancer therapy efficacy,

millions of patients today survive and live with a history of can-

20cer. For them, ESMO encourages oncologists, in partnership with

MDTs, to develop programmes of:

• Prehabilitation (at the time of diagnosis or relapse) to reducefrailty and prepare patients to receive adequate treatment.Prehabilitation may also reduce post-treatment disorders [27, 28].

Table 1. Key patient-centred care interventions (examples)

Assessment Monitoring and intervention:regular changes in patients’health status preferably assessedwith PROMs or other validatedassessment tools

Management of cancer-relatedsymptoms and other needs

Management of anticancertreatment-related toxicities andcomplications, includingprevention

• Cancer and anticancer-treatmentrelated symptoms, toxicities,complications

• Psychological disorders, distress• Sleeping problems• Spiritual and existential issues• Comorbidities• Nutritional status• Sexuality concerns• Prognosis and coping with

cancer disease• Family and/or caregiver issues• Socioeconomic issues• Other unmet needs

• Adverse events of anticancertreatment, specifically underimmunotherapy

• Compliance/adherence to onco-logic treatments (e.g. oral antineo-plastic agents)

• Frequency of unplanned visitsand/or unplanned hospitalisation

• Special survivors’ needs• Coping mechanisms• Understanding of illness, treatment

and care options• Patient and caregiver information

(including help from culturalmediators when needed)

• Treatment decision-making• Advance care planning• Preparation for end-of-life and

dying• Family distress and care-giving

roles• Professional support networks• Loss of autonomy• Distress• Existential, spiritual and religious

needs• Other monitoring and intervention

issues

• Pain• Fatigue• Nausea and vomiting• Constipation, diarrhoea• Anorexia, cachexia, early satiety• Dyspnoea/breathlessness• Hydro electrolytic disorders• Prevention of skeletal related

events in patients with bonemetastases

• Anxiety• Depression• Sleeping disorders• Evacuative paracentesis• Endurance, resistance and balance

training• Support in understanding the dis-

ease itself as well as the diagnosis,treatment options and prognosis

• Supporting decisional processes ofpatient and family

• Organising and coordinatingcommunity support networks

• Coping with life limitingexpectancies

• Other management issues

• Nausea and vomiting• Anaemia• Febrile neutropenia• Fatigue• Pain• Infections• Dermatotoxicity• Neurotoxicity• Immune-related adverse events• Diarrhoea/constipation• Mucositis• Renal impairment,• Cardiotoxicity• Problems with sexuality• Endocrine disorders• Arthralgia• Prevention of CTIBL• Prevention of infertility• Maintenance of central access

devices• Hydro electrolytic disorders• Other symptom management

issues

PROMs, patient-reported outcome measures; CTIBL, cancer treatment-induced bone loss.

CANCER DIAGNOSIS

CURATIVE PALLIATIVE

REHABILITATION*SURVIVORSHIP

END OF LIFE

Figure 1. Schematic diagram of the cancer pathway. *Rehabilitationmay also apply in the palliative setting.

Annals of Oncology Special Article

doi:10.1093/annonc/mdx757 | 3

• Rehabilitation to reduce acute and chronic disabilities due to anti-neoplastic treatments. The objective is to help patients becomeand remain independent and productive members of society, orto cope better with remaining limitations [29]. Rehabilitation,however, can also be applied in palliative situations.

• Survivor care plans, to support patients in recovering ‘well-5 being’ in their personal, professional and social lives, may

reduce the risk of recurrence and help manage chronic dis-ease, but further research is needed on how to apply them inclinical practice [30–32].

End-of-life care

10 Special attention should be paid to patients and their caregivers

when life prolonging treatment comes to an end. In order to help

them cope with this transition, advanced care planning [33] as a

tool should be used early in the course of palliative chemo and

radiotherapy. Near the end-of-life [34], particularly during the last

15 days, these plans need to be adapted to patients and family mem-

bers’ individual needs, based on an open communication about

the natural course of the disease and the dying process [35].

‘Advanced directives’ should be discussed when appropriate, at

any time in the disease trajectory, allowing patients to spell out

20 their wishes about end-of-life care ahead of time. Discussing the

patient’s status and prognosis can be challenging for professio-

nals, therefore communication skills are essential.

Oncologists should be prepared to respond to emotions and to dis-

cuss the possible outcomes of cancer, including death. Professionals

25 should be able to understand what matters most to patients and their

families, to explain options simply and clearly, to help patients antici-

pate and plan in a way that is respectful of their wishes. This includes

respecting the patient’s right to refuse treatment.

The UK’s National Institute for Health and Care Excellence

30 (NICE) offers useful guidelines for care, as well as for pharmaco-

logical and non-pharmacological interventions, in the last days of

life [34], although the UK health care system including hospices

may not be transferable to other countries.

Multidisciplinary teams

35 The list of professionals that compose an MDT caring for patients

includes several specialties. In summary, there should be medical

oncologists, palliative medicine specialists, nurses, tumour origin

specialists, radiation oncologists, surgeons, pharmacists, allied

healthcare professionals, clerics and volunteers involved. A more

40 extensive list of professions that may be included in the MDT is

provided in the online supplement (see supplementary Table S1,

available at Annals of Oncology online). Of course, not all patients

will need the involvement of all these professionals.

The composition of the MDT, as well as tasks and responsibil-

45 ities, will vary according to patient needs, resources and national

settings. Nevertheless, the team should encompass medical and

non-medical professionals that can take care of a wide variety of

physical, psychological, social and existential needs.

If, due to financial or organisational limitations, the cancer

50 centre does not have the necessary staff in-house to cater to all

patient needs, patients should be referred to other centres or to

individual, trained, professionals (such as physiotherapists or

psychologists) where they have access to necessary interventions.

It is important that the medical oncologist in charge of treatment55and care is also responsible for coordinating these interventions

and regularly evaluates the efficacy of patient-centred care [23].

Integrating healthcare resources

ESMO has a long-term commitment to advance the integration

of supportive and palliative care in oncology and to excellence in60all aspects of oncological care.

Integration is needed to coordinate care processes, including

establishing what health care resources are needed: ‘the correct

competence in the right place at the right time’. The concept of

integration of palliative care into oncology has received substantial65attention recently although there is still no consensus on a defini-

tion of ‘integration’. In a recent article, Hui and Bruera [36] sum-

marized 38 aspects of integration based on a systematic review,

which were classified under 5 categories (clinical structure, clinical

process, education, research and administration). Subsequently,70an international Delphi panel highlighted 13 criteria as major indi-

cators of integration which may be useful for benchmarking pallia-

tive care access across healthcare systems [37].

In order to improve the current situation, ESMO is committed

to expanding cooperation with other professional medical associ-75ations and organisations worldwide [such as the European

Association of Palliative Care (EAPC), the Multinational

Association of Supportive Care in Cancer (MASCC), etc.] and to

encourage and sustain supportive and palliative care develop-

ment through its ‘ESMO Designated Centre of Integrated80Oncology and Palliative Care’ programme [38, 39].

Adequate patient-centred care should be provided as part of

the global service of every hospital or clinic treating cancer

patients. Integrating patient-centred services is the best way to

ensure that they will be widely available and acceptable to profes-85sionals and patients alike. The Eligibility Criteria Checklist of the

ESMO Designated Centre of Integrated Oncology and Palliative

Care programme can be seen on the ESMO website [40].

Resources being limited, not all oncology centres will have an

extended MDT (and not all patients will need support) but, as a90minimum, regular routine patient assessment of physical and

psycho-social needs should be offered, as well as provision of

interventions, whether in-house or by referral to medical or non-

medical professionals.

Need for specific training in patient-centred

95care

ESMO is committed to specialised education supporting oncolo-

gists in a fast-changing professional environment. The society

aims to help oncologists gain in-depth, disease-specific knowl-

edge as well as learning how to collaborate effectively with other100specialists in an integrated, multi-professional setting.

Medical oncologists should be trained in the supportive and

palliative care of patients, including basic knowledge about physi-

cal, psychological, social and spiritual aspects of cancer, as set out

in the ESMO/ASCO Recommendations for a Global Curriculum

Special Article Annals of Oncology

4 | Jordan et al.

in Medical Oncology (see Table 2) [41]. As such a structured rota-

tion in supportive and palliative care for oncology trainees would

be a helpful approach. Furthermore, as stated in 2003, ESMO con-

siders oncologists ‘should be familiar with the roles of other profes-5 sions in the care of patients with cancer and with community

resources to support the care of these patients’. If specialist patient-

centred care is required, oncologists should be able to identify

which appropriate professional the patient should be referred to.

National Societies should also promote continuing medical10 education (CME) in the basics of patient-centred care, to ensure

professionals learn about new developments in the field.

Requirements of the ESMO/ASCO Curriculum are addressed

in the following sections:

• Complications/toxicities of anticancer treatment.• Supportive care measures.• Palliative care.• End-of-life care.

The objectives encompassed are shown in Table 2.

15 ESMO resources for integrated patient-

centred care education

ESMO already offers a wide array of educational programmes

and tools to oncologists in the domain of patient-centred care

(see Table 3).

20 Research needs and resources in supportive

and palliative care

Despite growing awareness of the need to develop patient-cen-

tred care and recent progress in the field, more and better scien-

tific evidence, tailored to individual and fluctuating patient needs25 is required so that effective interventions can be proposed to can-

cer patients at each stage of their illness.

Prospective, well-designed and preferably, intervention studies

are needed to evaluate the impact of palliative and supportive

interventions on outcomes and QoL. Even in pain management30 the level of evidence in existing guidelines is low [42–44]. In this

area, the ESMO-led Global Opioid Policy Initiative (GOPI) [45]

seeks to drive necessary policy reform to improve severe cancer

pain management and unnecessary suffering. It calls for author-

ities to guarantee the availability and accessibility of effective and35 safe pain killing treatments.

ESMO is willing to promote more research fellowships in sup-

portive and palliative care. Research in patient-centred care should

be the focus of original investigation. For anticancer treatment tri-

als, PROs should be used together with traditional tumour-ori-40 ented outcomes. It is not enough to include QoL measures in

cancer clinical trials as secondary or tertiary outcomes.

Often, only research validated by RCTs is considered accept-

able. Nevertheless, there are methodological and ethical issues

[46] linked to RCTs in palliative and end-of-life care (i.e. con-45 cerns about informed consent and the vulnerability of patients).

However, recent RCTs in this setting and embedded in qualitative

work showed that patients with advanced cancer benefit from

participation in symptom control trials [47, 48].

Other options include well-designed observational studies and50cross-sectional surveys [49]. More research is needed, for exam-

ple, on short- and long-term side-effects of new therapeutic inter-

ventions [50]; new supportive care agents; integrating new

technologies such as a web-based programmes and apps for self-

monitoring and reporting symptoms; congruent outcome assess-55ments on symptoms and side-effects (health care assessment ver-

sus PROs); nutrition, physical activity, QoL; social factors such as

family issues, social support, work, financial toxicity; care giver

attitudes and practices; rehabilitation and survivor care; identify-

ing organisational, economic and other incentives for the provi-60sion of integrated and affordable patient-centred care.

ESMO calls for more research to be carried out in this area in

order to create the evidence needed to improve patient-centred

care. Furthermore, a pragmatic approach to cancer research is

needed where patient-centred care trials are concurrent with can-65cer therapy trials.

Table 2. Requirements of the ESMO/ASCO Curriculum

• To be able to assess, diagnose and treat patients with complications/toxicities of anticancer therapies

• To be able to understand, evaluate and provide supportive careto patients with cancer, including management of symptoms from thecancer and side-effects of therapy from the time of diagnosis untildeath or until rehabilitation and survivorship issues have beensuccessfully managed

• To know the indications for the different supportive treatments andtheir limitations and side-effects

• To be aware of the importance of a multidisciplinary approach• To be able to screen for, assess, prevent and manage symptoms

of patients with cancer such as pain, fatigue, anorexia, anxiety,depression, breathlessness and nausea

• To communicate effectively with patients and families aboutillness understanding and coping with it, prognosis, difficult decisions,end-of-life and its preparation

• To recognise the role of cancer rehabilitation, including physicaltherapy and nutrition

• To recognise the importance of culturally competent,multidisciplinary care including families

• To understand how to integrate palliative interventions in routinemultidisciplinary cancer care

• To recognise the difference between burnout, compassion fatigueand depression

• To recognise the unique aspects of end-of-life care, such asdecision-making processes, symptom management, involvement offamily members andspiritual aspects

• To understand how to recognise pseudo-refractory symptoms andwhen to refer to specialist palliative care teams for management ofrefractory symptoms

• To understand how to maintain patients’ cognition until close todeath with good symptom control

• To be able to assess, treat and counsel patients who areapproaching end-of-life

• To incorporate the family and beloved ones into goal planning• The curriculum also defines the required skills in dealing with the

psychosocial aspects of cancer, geriatric oncology, communication,patient education and survivorship.

Annals of Oncology Special Article

doi:10.1093/annonc/mdx757 | 5

Future/vision

ESMO is committed to ensuring that patient-centred care is

widely understood and integrated into health systems at all levels

throughout the disease; that oncologists have the necessary5 knowledge and skills (competences) and that it is underpinned

by a high level of evidence. Therefore, ESMO will advocate for

• increased awareness;• increased research;• increases education; and• increased resources to be dedicated to supportive and pallia-

tive care.

ESMO appeals to health authorities in Europe and beyond to

ensure that cancer patients have equal access to the best possible10 patient-centred cancer care that resources allow. This is a medical

and ethical imperative.

Discussion

Conclusion

Recent studies show variable effects of the integration of early15 supportive and palliative care interventions for cancer patients

and also emphasise their importance. The diverse outcomes may

be partly explained by methodological challenges, i.e. different

interventions, outcomes and patient populations applied in

published RCTs. Manifestly, more research is needed in patient-20 centred care.

Together with anticancer therapies, medical oncology should

encompass patient-centred care by providing supportive and

palliative interventions at all stages of the disease, from the time

of diagnosis. The oncologist’s role is not only to deliver the best

25quality anticancer treatment, but also to consider the impact of

the disease and treatment on each patient’s life. Oncologists

should be responsible for including and collaborating with

health care providers with other competences in outpatient and

inpatient clinics in order to alleviate patients’ distress. Since

30only individual patient needs can determine what support is

required at each stage of the disease, it is challenging to define

models and standards for best patient-centred care, neverthe-

less, interventions should be based on the best available

evidence.

35Further research is needed to ensure that palliative and suppor-

tive interventions are evidence based and PROs should be highly

encouraged. CME is also essential for oncologists to acquire and

update the necessary skills to evaluate patients’ specific needs and

provide the best care.

40ESMO is committed to ensuring that supportive and palliative

care is widely understood, integrated into health systems at all

levels and underpinned by evidence.

Acknowledgement

The authors thank Jackie Partarrieu from the ESMO Press

45Office for the editorial assistance during the preparation of the

manuscript.

Table 3. ESMO resources for integrated patient-centred care education

• E-learning modulesa on supportive and palliative care• ESMO Palliative Care Fellowshipsb ESMO provides two palliative care fellowships allowing recipients observation or research at one of the ESMO

Designated Centres• ESMO Clinical Practice Guidelinesc including guidelines on supportive care and palliative care.• ESMO Patient Guidesd include, e.g. how to deal with side-effects• ESMO Handbooks for physicianse

• ESMO Academyf includes an overview of standards of care and future perspective in supportive care• ESMO Preceptorships in supportive care and palliative careg

• Oncology Pro Webcasts and Slides, Scientific Meeting Reports (using search function) http://oncologypro.esmo.org/Slide-Resources• ESMO Congress track on supportive care and palliative care• Core Curriculum slide sets: http://www.esmo.org/Career-Development/Global-Curriculum-in-Medical-Oncology• ESMO collaboration with other entities with interest in supportive care and palliative care (e.g. MASCC, EAPC, ESO)• Other resources on the ESMO website: http://www.esmo.org/Topics/Palliative-and-supportive-care

aESMO e-learning: http://oncologypro.esmo.org/Science-Education/ESMO-E-Learning-and-V-Learning.bESMO Fellowships: http://www.esmo.org/Career-Development/Oncology-Fellowships/Awardees-and-Reports/Palliative-Care-Fellowship-Reports.cESMO Guidelines on Supportive Care: http://www.esmo.org/Guidelines/Supportive-Care.dESMO Patient Guides: http://www.esmo.org/Patients/Patient-Guides and ESMO Guide for Patients with Advanced Cancer http://www.esmo.org/content/download/6932/132781/file/ESMO-A-Guide-for-Patients-with-Advanced-Cancer.pdf.eESMO Handbooks: (i) http://oncologypro.esmo.org/Publications/Handbooks/Nutrition-and-Cancer; (ii) http://oncologypro.esmo.org/Publications/Handbooks/Advanced-Cancer-Care III. http://oncologypro.esmo.org/Publications/Handbooks/Rehabilitation-Issues-During-Cancer-Treatment-and-Follow-Up.fESMO Academy: http://www.esmo.org/Conferences/ESMO-Academy-2017/Programme.gESMO Preceptorship. Slides from the 2017 preceptorship on supportive and palliative care http://oncologypro.esmo.org/Meeting-Resources/ESMO-Preceptorship-on-Supportive-and-Palliative-Care-Zurich-February-2017.

Special Article Annals of Oncology

6 | Jordan et al.

Funding

None declared.

Disclosure

KJ: Advisory board and or honoraria for presentations for5 Merck, MSD, Helsinn, Tesaro, Amgen, Hexal, Pfizer.

MA: Grant/Reserch supports: Amgen, Eisai, Genomic Health,

Helsinn, Hospira, Novartis, Merck, Mundipharma, Pfizer,

Roche, Sandoz, Tesaro, Teva, Vifor. Consultant for Amgen,

BMS, Celgene, Clinigen, Eisai, Genomic Health, GSK, Helsinn,10 Hospira, JnJ, Novartis, Merck, Merck Serono, Mundipharma,

Pfizer, Pierre Fabre, Roche, Sandoz, Tesaro, Teva, Vifor and has

received honoraria for lectures at symposia (equivalent speaker’s

bureau) of Amgen, Bayer Schering, Cephalon, Chugai, Eisai,

Genomic Health, GSK, Helsinn, Hospira, Ipsen, JnJ,15 OrthoBiotech, Kyowa Hakko Kirin, Merck, Merck Serono,

Mundipharma, Novartis, Pfizer, Pierre Fabre, Roche, Sandoz,

Sanofi, Tesaro, Taiho, Teva, Vifor.

SK: Holds stocks in EIR Solutions.

CIR: Honoraria from Amgen for educational programs on ONJ.20 FS: Roche, Vifor, MSD, Teva, Norgine, Prostrakan, Leo pharma,

Janssen, Hospira, Boehringer, Sanofi, AMGEN, Pierre Fabre

Oncologie, Tesaro.

FS: Unrestricted Industry Grants for Clinical Research (last

10 years) Celgene (Lenalidomide Cachexia trial) Fresenius25 (Survey parenteral nutrition malignant bowel obstruction)

Helsinn (Palliative Research Centre, MENAC Trial, KSSG

Cachexia) Participation in company-lead clinical cachexia trials

Novartis (BYM338 cachexia trial) Punctual Advisorship

(Boards, Expert Meetings) Acacia, ACRAF, Amgen, Baxter,30 Celgene, Danone, Fresenius, GlaxoSmithKline, Grunenthal,

Helsinn, ISIS Global, Millennium/Takeda, Mundipharma,

Novartis, Novelpharm, Nycomed, Obexia, Otsuka, Ono,

Pharm-Olam, Pfizer, Psioxus, PrIME, Santhera, Sunstone, Teva,

Vifor. Honoraria for Speaking Helsinn prIME.35 AY: Honoraria from MSD, Helsinn, Bayer, Leo Pharma.

Educational grant from Bayer.

EB: Research grant from Helsinn Pharma.

JH: Advisory board activity Tesaro and remuneration SOBI.

DK: Advisory Board and stock options: Entrinsic Health40 Solutions. Advisory Board: Second Genome.

BL: Advisory Board for Pfizer and Chugai Pharma.

DW: Non-executive Director of Nualtra.

J-YD has declared no conflicts of interest.

AC: Advisory board and or honoraria for Amgen, Lilly,45 Novartis, Takeda, Roche, MerckSerono, Servier.

References

1. Torre L, Bray F, Siegel R et al. Globocan Global cancer statistics, 2012.

(2015) Global cancer statistics. CA Cancer J Clin 2015; 65(2): 87–108;

http://onlinelibrary.wiley.com/doi/10.3322/caac.21262/full (29 November50 2017, date last accessed).

2. Cherny N, Sullivan R, Dafni U et al. A standardised, generic, validated

approach to stratify the magnitude of clinical benefit that can be antici-

pated from anti-cancer therapies: the European Society for Medical

Oncology Magnitude of Clinical Benefit Scale (ESMO-MCBS). Ann55 Oncol 2015; 26(8): 1547–1573.

3. Velikova G, Coens C, Efficace F et al. Health-related quality of life in

EORTC clinical trials: 30 years of progress from methodological develop-

ments to making a real impact on oncology practice. Eur J Cancer 2012;

10(1): 141–149.604. Laird B, Fallon M, Hiermstad S et al. Quality of life in patients with

advanced cancer: differential association with performance status and

systemic inflammatory response. J Clin Oncol 2016; 34(23): 2769–2775.

5. Cherny N, Catane R, Kosmidis P. ESMO takes a stand on supportive and

palliative care. Ann Oncol 2003; 14(9): 1335–1337.656. Hui D, Mori M, Parsons HA et al. The lack of standard definitions in the

supportive and palliative oncology literature, 2012. J Pain Symptom

Manage 2012; 43(3): 582–592.

7. WHO Definition of Palliative Care, World Health Organization.

Factsheet n.402, July 2015; http://www.who.int/mediacentre/factsheets/70fs402/en/ (29 November 2017, date last accessed).

8. Radbruch L, Payne S. White paper on standards and norms for hospice

and palliative care in Europe: Part 1. Eur J Palliative Care 2009; 16(6):

278–289.

9. Consensus on the Core Ideology of MASCC. Definition of Supportive75Care; http://www.mascc.org/index.php? option¼com_content&view¼

article&id¼493: mascc-strategic-plan&catid¼30: navigation (29 November

2017, date last accessed).

10. Zimmermann C, Swami N, Krzyzanowska M et al. Perceptions of pallia-

tive care among patients with advanced cancer and their caregivers.80CMAJ 2016; 188(10): E217–E227.

11. Frampton S, Guastello S, Brady C et al. Patient Centered Care

Improvement Guide. Planetree, Inc. and Picker Institute. 2008; http://

www.ihi.org/resources/Pages/Tools/PatientCenteredCareImprovement

Guide.aspx (29 November 2017, date last accessed).8512. WHO Framework on integrated people-centred health services; http://

apps.who.int/gb/ebwha/pdf_files/WHA69/A69_39-en.pdf? ua¼1&ua¼1

(29 November 2017, date last accessed).

13. Basch E, Deal AM, Dueck AC et al. Overall survival results of a trial

assessing patient-reported outcomes for symptom monitoring during90routine cancer treatment. JAMA 2017; 318(2): 197–198.

14. World Health Organization. Strengthening of palliative care as a compo-

nent of integrated treatment throughout the life course. J Pain Palliative

Care Pharmacother 2014; 28(2): 130–134.

15. Kavalieratos D, Corbelli J, Zhang D et al. Association between palliative95care and patient and caregiver outcomes. A systematic review and meta-

analysis. JAMA 2016; 316(20): 2104–2114.

16. Haun MW, Estel S, Rucker G et al. Early palliative care for adults with

advanced cancer. Cochrane Lib 2017, Issue 6. Art. No.: CD011129. doi:

10.1002/14651858.CD011129.pub210017. Gaertner J, Siemens W, Meerpohl J et al. Effect of specialist palliative care

services on quality of life in adults with advanced incurable illness in

hospital, hospice, or community settings: systematic review and meta-

analysis. BMJ 2017; 357:j2925. doi: https://doi.org/10.1136/bmj.j2925.

18. Groenvold M, Petersen MA, Damkier A et al. Randomised clinical trial105of early specialist palliative care plus standard care versus standard care

alone in patients with advanced cancer: the danish palliative care trial.

Palliat Med 2017; 31(9): 814.

19. Franciosi V, Caruso G, Maglietta G et al. Palliative care evaluation of

effects early palliative care on quality of life of advanced cancer patients:110a multicenter controlled trial. Ann Oncol 2016; 27(Suppl 6): LBA49.

20. Ripamonti C, Pessi MA, Boldini S et al. Supportive Care in Cancer Unit

(SCCU) at the NCI of Milan: a new integrated model of medicine in

oncology. Curr Opin Oncol 2012; 24: 391–396.

21. Scotte F, Herve C, Oudard S et al. Supportive care organisation in115France: an in depth study by the French speaking association for suppor-

tive care in cancer (AFSOS). Eur J Cancer 2013; 49(5): 1090–1096.

22. Vasile E, Lucchesi M, Ginocchi L et al. Dedicated supportive care team at

the oncology unit: a model of simultaneous care for cancer patients.

Support Care Cancer 2014; 22(4): 867–868.12023. Scotte F, Herve C, Leroy P et al. Supportive Care Organization in France:

a national in-depth survey among patients and oncologists. Support

Care Cancer 2017; 25(7): 2111–2118.

Annals of Oncology Special Article

doi:10.1093/annonc/mdx757 | 7

24. Antonuzzo A, Vasile E, Sbrana A et al. Impact of a supportive care service

for cancer outpatients: management and reduction of hospitalizations.

Preliminary results of an integrated model of care. Support Care Cancer

2017; 25(1): 209–212.5 25. Ripamonti CI, Molani P, Desti C et al. A supportive care in cancer unit

reduces costs and hospitalizations for transfusions in a comprehensive

cancer center. Tumori 2017; 103(5): 449–456.

26. Morin S, Leroy P, Aubaret C et al. Cost effectiveness in a supportive

care unit. J Clin Oncol 2017; 35 (suppl; abstr e18326). https://meetingli

10 brary.asco.org/record/152502/abstract (29 November 2017, date last

accessed).

27. Skinner EH. Intensive preoperative rehabilitation improves functional

capacity and postoperative hospital length of stay in elderly patients with

lung cancer [synopsis]. J Physiother 2017; 63(3):184.15 28. Driessen EJ, Peeters ME, Bongers BC et al. Effects of prehabilitation and

rehabilitation including a home-based component on physical fitness,

adherence, treatment tolerance and recovery in patients with non-small

cell lung cancer: a systematic review. Crit Rev Oncol Hematol 2017; 114:

63–76.20 29. O’Mara A, Rowland JH, Greenwell TN et al. NIH Medical Rehabilitation

Coordinating Committee. National Institutes of Health Research Plan

on Rehabilitation: NIH Medical Rehabilitation Coordinating

Committee. Phys Ther 2017; 97(4): 104–407.

30. Leensen MCJ, Groeneveld IF, Heide IV et al. Return to work of cancer

25 patients after a multidisciplinary intervention including occupational

counselling and physical exercise in cancer patients: a prospective study

in the Netherlands. BMJ Open 2017; 7(6): e014746.

31. Leensen MCJ, Groeneveld IF, Rejda T et al. Feasibility of a multidiscipli-

nary intervention to help cancer patients return to work. Eur J Cancer30 Care (Engl) 2017; doi:10.1111/ecc.12690.

32. ESMO Patient Guide on Survivorship; http://www.esmo.org/content/

download/117593/2061518/file/ESMO-Patient-Guide-Survivorship.pdf

(29 November 2017, date last accessed).

33. Schrijvers D, Cherny N. ESMO Clinical Practice Guidelines on

35 palliative care: advanced care planning. Ann Oncol 2014; 25(Suppl 3):

iii138–iii142.

34. End of life care. NHS; http://www.nhs.uk/Planners/end-of-life-care/

Pages/what-is-end-of-life-care.aspx (29 November 2017, date last

accessed).40 35. Care of adults in the last days of life. NICE guideline. December 2015;

https://www.nice.org.uk/guidance/ng31/resources/care-of-dying-adults-

in-the-last-days-of-life-pdf-1837387324357 (29 November 2017, date

last accessed).

36. Hui D, Bruera E. Integrating palliative care into the trajectory of cancer45 care. Nat Rev Clin Oncol 2016; 13: 159–171.

37. Hui D, Bansal S, Strasser F et al. Indicators of integration of oncology

and palliative care programs: an international consensus. Ann Oncol

2015; 26(9): 1953–1959.

38. The ESMO Designated Centres of Integrated Oncology and Palliative Care50accreditation programme; http://www.esmo.org/Patients/Designated-

Centres-of-Integrated-Oncology-and-Palliative-Care (29 November 2017,

date last accessed).

39. Hui D, Cherny N, Latino N, Strasser F. The 0critical mass0 survey of pal-

liative care programme at ESMO designated centres of integrated oncol-55ogy and palliative care. Ann Oncol 2017; 28(9): 2057–2066.

40. http://www.esmo.org/Patients/Apply-to-Become-an-ESMO-Designated-

Centre (29 November 2017, date last accessed).

41. Recommendations for a Global Curriculum in Medical Oncology; http://

www.esmo.org/Career-Development/Global-Curriculum-in-Medical-60Oncology (29 November 2017, date last accessed).

42. Caraceni A, Hanks G, Kaasa S et al. Use of opioid analgesics in the treat-

ment of cancer pain: evidence-based recommendations from the EAPC.

Lancet Oncol 2012; 13(2): e58–e68.

43. Ripamonti CI, Bossi P, Santini D, Fallon M. Pain related to cancer treat-65ments and diagnostic procedures: a no man’s land? Ann Oncol 2014;

25(6): 1097–1106 (review).

44. Bandieri E, Romero M, Ripamonti CI et al. Randomized trial of low-

dose morphine versus weak opioids in moderate cancer pain. J Clin

Oncol 2016; 34(5): 436–442.7045. ESMO-led Global Opioid Policy Initiative (GOPI); http://www.esmo.

org/Policy/Global-Opioid-Policy-Initiative (29 November 2017, date last

accessed).

46. Hanks G. Ethical issues in palliative care research. In The Oxford Textbook

of Palliative Medicine 2010; Oxford, UK: Oxford University Press. DOI:7510.1093/med/9780199656097.001.0001. http://oxfordmedicine.com/view/

10.1093/med/9780199656097.001.0001/med-9780199656097-chapter-196

(29 November 2017, date last accessed).

47. Fallon M, Hoskin PJ, Colvin LA et al. Randomized double-blind trial of

pregabalin versus placebo in conjunction with palliative radiotherapy for80cancer-induced bone pain. JCO 2016; 34(6): 550–556.

48. Solheim TA, Laird BJA, Balstad TR et al. A randomised phase II trial of a

multimodal intervention for the management of cachexia in lung and

pancreatic cancer. J Cachexia Sarcopenia and Muscle 2017; 8: 778–788.

49. Middlemiss T, Lloyd-Williams M, Laird BJ et al. Symptom control trials85in patients with advanced cancer: a qualitative study. J Pain Symptom

Manage 2015; 50(5): 642–649.

50. A Beginners Guide to Successful Palliative Care. Scottish Partnership for

Palliative Care. Section 5: Identifying potentially useful ideas for research;

https://www.palliativecarescotland.org.uk/content/publications/134028908254_A-Beginners-Guide-to-Successful-Palliative-Care-Research-.pdf

(29 November 2017, date last accessed).

Special Article Annals of Oncology

8 | Jordan et al.