With the groundbreaking work of three Milan professors—Bonadonna, Veronesi, and Ventafridda—in the 1980s as the starting point, this article aims to shed light on the potential benefits of a closer and more formal integration between oncology and palliative care. More specifically, we address why integration is needed, how to do it, and the potential benefits to the patients, families, and society. The costs for cancer care are increasing rapidly. Especially during the last year of life, some treatments are futile and expensive without proven benefit for patients in terms of prolonged survival with adequate quality of life (QoL). The latest WHO definition of palliative care supports an upstream introduction of palliative care. More recent studies indicate that such an early integration has the potential to improve the patients’ QoL and reduce their symptom burden. Successful integration presupposes formal structures and explicit obligations on how and when to integrate. The Norwegian model for palliative care is presented. It covers the range of oncologic and palliative services from community health care via the local hospital to the tertiary hospital and rests on standardized care pathway as the key instrument to promote integration. Our present state of knowledge indicates that integration does not shorten life; perhaps even the opposite. Futile oncological treatment can be reduced and the QoL of patients and carers improved. We need more evidence on the potential effect upon costs, but present data indicate that integration does not increase them.
Tumori 2017; 103(1): 1 - 8
Article Type: REVIEW
AuthorsStein Kaasa, Anne Kari Knudsen, Tonje Lundeby, Jon Håvard Loge
- • Accepted on 21/12/2016
- • Available online on 12/01/2017
- • Published in print on 21/01/2017
This article is available as full text PDF.
In 1983, Stein Kaasa started his training in medical oncology and radiotherapy at the Norwegian Radium Hospital, Oslo, Norway. At that time, there were vigorous discussions during and after the demonstration of the x-rays of the patients. The head of the department, Prof. H. Høst, who is a well-cited clinical scientist in oncology (1), continuously referred to “the Milan breast cancer group” and specifically to the medical oncologist Prof. G. Bonadonna (2). To be trained in oncology at that time and not aware of adjuvant treatment for breast cancer with cyclophosphamide, methotrexate, and 5-fluorouracil, invented and proven to be effective in high-quality clinical trials, would have been unacceptable (3, 4).
Later, during Kaasa’s first years as a junior doctor, there were also intensive discussions about surgery for breast cancer patients. A second pioneer from the Milan group, Prof. U. Veronesi, a surgeon, was also outstanding in the world of breast cancer care. With the same spirit, he pushed the field of breast cancer care with innovative approaches, like Prof. Bonadonna, by systematically evaluating new surgical techniques for breast cancer care “from mastectomy to quadrectomy” (5).
Some years later, in 1992, after Kaasa had finished his training in oncology and a PhD thesis in medicine focusing on quality of life (QoL) in lung cancer patients, he met Prof. V. Ventafridda for the first time at a European Association for Palliative Care (EAPC) congress in Brussels. Prof. Ventafridda was a pioneer in palliative medicine and palliative care, initiated the palliative care program at the Istituto Nazionale dei Tumori (INT) in Milan, and was the founder of the EAPC in 1987, and one of the inventors of the WHO pain ladder (6, 7).
To our understanding, these are the similarities and differences among the three outstanding clinicians, researchers, and innovative thinkers from INT in Milan working together in the same period:
Leaders in their fields
Brought cancer care to new heights
Performed clinical trials systematically to prove the clinical benefits of new treatments
Had a clear focus in their approaches (although they had different foci: the chemotherapy approach, the surgical approach, and the palliative care approach)
More than 25 years ago, the link between the chemotherapy/radiotherapy approach and the palliative care approach was not evident. At that time, it was argued that palliative care (starting with hospice care in the mid-1960s) had a holistic approach, also named the total pain approach, in contrast to the more narrow-minded oncology approach, primarily focusing on the tumor and how the tumor could be treated (8).
In 2017, patients, families, and society are expecting more from modern cancer care than a narrow-minded approach. Expectations go in the direction of higher cure rates (reduced cancer-related mortality), as Bonadonna significantly contributed to by the adjuvant chemotherapy approach; improved survival; to live longer with the disease as well as improved quality of life (i.e., symptom control, sustainability of physical function, coping with the disease and the accompanying psychological challenges); patients being involved in decision-making; better end-of-life care; and better care for the family after death of the patients.
If these issues had been on the arena in the 1980s-1990s, the Milan trio Bonadonna, Veronesi, and Ventafridda would probably have taken the international lead also in this area of cancer care: the integration or the complementarity of mainstream oncology and palliative care.
The aim of this article is to shed light on the potential benefits of a closer and more formal integration between oncology and palliative care in special cancer care centers. More specifically, we address why integration between oncology and palliative care is needed, how to do it, and what are the potential benefits to patients, families, and society.
Why is integration between oncology and palliative care needed?
Cancer incidence and prevalence are steadily increasing and are expected to continue to increase in the forthcoming decades (9). In 2012, 2.45 million new patients were diagnosed with cancer in 40 European countries, and 1.75 million patients died from cancer (10).
Trends in incidence, mortality, and survival in Norway. From Cancer in Norway 2015. With permission from the Norwegian Cancer Registry.
The major driver for the increasing incidence and the accompanying increase in prevalence is the aging population. For many patients, cancer has become a chronic disease, either due to late or long-term effects or due to an increased number of treatment lines that prolong life but do not cure the disease. The proportion of the total cancer population belonging to the latter category is unclear, but the number is increasing based upon observations of the enrolled patients at our hospital. Caring for them is often resource-consuming in terms of diagnostic tests and treatments. Further, many of the patients present with complex problems related to the disease and the treatment, such as bothersome symptoms or psychosocial problems. The latter might include problems with psychological adaptation, family function, and work-related problems. Adding this to a stable number of deaths from cancer, the need for palliative care is expected to increase in the years ahead.
As long as the treatment intention is curative, we find it pertinent to use the term supportive care for interventions that might also be core parts of palliative care such as pain relief. We thereby adhere to the latest WHO definition of palliative care, defining palliative care as “an approach that improves the QoL of patients and their families facing the problems associated with life-threatening illness, through the prevention and relief of suffering by means of early identification and impeccable assessment and treatment of pain and other problems, physical, psychosocial and spiritual” (12). Interestingly, the WHO definition also points to an early integration of oncology and palliative care by stating that “palliative care is applicable early in the course of illness, in conjunction with other therapies that are intended to prolong life, such as chemotherapy or radiation therapy, and includes those investigations needed to better understand and manage distressing clinical complications.”
Best possible QoL is the main goal of palliative care. Optimal symptom management is the primary means to achieve it. Still, the ambiguous concept of QoL is not defined by the WHO definition, leaving its content open to interpretation. In line with the 2006 Food and Drug Administration guideline, we define QoL as “a general concept that implies an evaluation of the impact of all aspects of life on general well-being” (13). Furthermore, the WHO definition of palliative care also states that “palliative care affirms life and regards dying as a normal process.”
These definitions illustrate that oncology and palliative care have supplementary goals: disease control as the main goal of oncology and best possible QoL for the patients and their families as the main goal of palliative care. This implies that integration can be a feasible approach for providing the best care for patients with cancer. In the clinical context, the main question for the oncologist is to decide when specialist care is needed for symptom management during curative treatment and when the cancer-directed treatment no longer gives the patient the life prolongation as expected from the trials upon which the treatment is based, or when the treatments’ negative impact on QoL overweighs the gain in expected survival. Basically this is a question about prognostication, which is a challenging task for the treating physician (14). For palliative care, intervening early implies that this care also needs to know the evidence base for the oncologic treatment and also the expected disease trajectories of their patients in order to provide optimal care that improves or maintains the QoL of their patients irrespective of their prognosis.
Apart from the definitions described above, which point to integration as a desired approach, there are other factors that have made integration of oncology and palliative care a topical issue in present oncology. These are reflected in the American Society of Clinical Oncology’s (ASCO) provisional clinical opinion (15), recently being developed into an updated ASCO guideline (16). These statements were partially based on normative grounds. They may also be understood in light of societal needs such as reducing costs and upon developments within oncology and palliative care as such.
The rapidly increasing complexity of oncological treatment implies a considerable increase in costs of care. This increase threatens the sustainability of present health care services in general, but specifically in cancer care (17). The increasing use of chemotherapy and radiotherapy and advanced imaging (computed tomography [CT]/magnetic resonance imaging/positron emission tomography CT) during the last 12 months of life has led to escalating costs and high treatment complexity, despite insufficient documentation of efficacy. In a recent published national French study, all patients with cancer in a given time period who received chemotherapy were analyzed. Very high rates of use of chemotherapy were found: 39% received chemotherapy during the last 3 months of life and 20% and 11% in the last month and the last 2 weeks of life, respectively (18).
For the treating oncologist, this is a challenge. A recent article examined the rationale for discontinuation of chemotherapy for metastatic non-small-cell lung cancer and identified a large variability in these processes, unrelated to time of death (19). This is in contrast to the fact that patients, families, and oncologists are recognizing the administration of chemotherapy near death as futile and an indicator of poor end-of-life care (20). Although it is challenging to study this topic with robust methodology, there are clear indications that patients who receive intensive treatment at end of life have poorer QoL compared with those receiving symptomatic treatment only (21).
Some studies indicate that early introduction of palliative care to patients with unfavorable prognosis may improve their QoL, enhance symptom control (22), and also possibly lead to prolonged survival (23). The interventions also point to integration as a means to give patients and carers a more realistic perspective on the disease and prognosis (23-24-25).
Despite rapid development of palliative care services during the last 15-20 years, there is still a distinct separation between oncology and palliative care in many Western countries (26). Palliative care provision is heterogeneous, often delivered in separate departments or even outside the hospitals at which the oncological treatment is delivered. In order to deliver personalized care when the patients are still receiving cancer-directed therapy, palliative care must be where the patients are. Palliative care models applied in studies of integration with oncology address a spectrum of symptoms/issues than cannot easily be handled in a busy oncologic outpatient setting.
Information given to cancer patients and carers about the disease, its treatment, and expected results is important at all stages of disease. Such information is especially crucial when life expectancy is limited as it may facilitate shared decision-making and thereby improve satisfaction with care and patients’ sense of control in a vulnerable phase of life. An explicit sharing of caring obligations can improve the care by a shared and structured commitment between oncology and palliative care for the patients prior to the traditional end-of-life phase.
How to do it?
Given the increasing complexity of treatments, physicians face an increasing number of treatment choices that often have to be made based upon their individual evaluation of each given clinical situation. Such evaluations may be limited by the individual physician’s skills and his or her professional environment. The well-known difficulties related to changing established practice based upon studies, reviews, and guidelines must be understood in light of individual, systemic, and cultural factors. Therefore a stronger focus upon the implementation of new knowledge and how this can change practice is warranted. In the context of integrating palliative care and oncology, having the opportunity to refer to palliative care is probably not enough to ensure that each individual patient experiences the benefits of both oncology and palliative care. Perceived time constraints, personal attitudes and preferences, established routines, and professional subcultures are some factors that explain the low referral rates to palliative care in many hospitals having both services available. In our view, a structured and more transparent approach is therefore needed. Standardized care pathways is such an approach giving the opportunity to combine clear definitions of professional tasks and obligations at defined time points with best available evidence.
Intensity of symptoms and level of functions may vary over time during the cancer disease trajectory and with different treatments. Therefore it is necessary to have a dynamic structure to improve QoL of the patients. The organizational structure of health care services should address the dynamic needs of patients and palliative care services should be available to the patients during life-prolonging treatments and also for all patients during curative treatment in order to alleviate symptoms and to deliver psychosocial support during and after treatment.
In order to apply to the content and to set a new structure in cancer care, some modifications of thinking and structure are needed.
Key elements for the content and structure of integrated cancer palliative care
|Improve overall quality of life|
|Assess and treat symptoms|
|Improve or maintain function|
|Address death as a normal process|
|Offer palliative care early in disease/treatment trajectories|
|Make reliable plans for the patients|
|Use standardized care pathways|
|Set a flexible organization of the health care system|
A model of early and integrated oncology palliative care: Norwegian experience with Italian help
The development of this structure of integrated cancer palliative care has evolved over years. In Norway, it started in 1993, when the palliative care program was launched at the university hospital in Trondheim and evaluated in a cluster randomized trial (24, 27) inspired by the work at INT in Milan and in Edmonton, Canada, in the early 1990s (28, 29). In this first model of care, the palliative medicine unit (PMU) consisted of a 12-bed inpatient acute unit, an outpatient clinic, and an ambulatory team available at all parts of the hospital. In order to make the model sustainable from both an economic and professional competence point of view, the PMU was established as an integrated structure within the department of oncology. The consequence was that the inpatient and outpatient activities were organized independently from mainstream oncology in the daytime where physicians on call could be from either the PMU or the department of oncology. Four key elements constituted the program: (1) inpatient and outpatient hospital palliative care provided by the PMU; (2) strengthened collaboration with community care services including general practitioners; (3) guidelines for continuous interaction between hospital and community care; and (4) educational program for community care professionals.
This model was later further developed in Norway as described in
Organizational model of oncology and palliative care in Norway.
For oncology, this means that the healthcare authorities have asked for establishment of palliative care programs at all four university hospitals in Norway, at local hospitals, and at the community care level. This model is further supported by the latest national cancer strategy for Norway 2013-2017 (32). Here it is stated that palliative care should be an integrated part of the cancer care pathways. Furthermore, it is stated that Norway will be a leading country in the use of standardized care pathways (32).
At the early stage in the 1990s, competence in palliative care in Norway was not formalized and the physicians both in hospital and community care had to receive training from formal and informal courses, tutorships, and visits at international palliative care programs. Later, in the Nordic countries, education in palliative medicine was formalized through the establishment of a Nordic course in palliative medicine (33) and since 2011 formalized as a built-upon specialty in Norway (34). This formal education was based on a holistic philosophy with a multidisciplinary approach to address patients’ and their families’ needs.
A structure of integration between clinical practice and research
As in medicine in general, the goal with palliative care is to conduct evidence-based clinical practice. In order to reach this goal, it is paramount that clinical care is totally integrated with clinical research. This model is to a certain extent mirroring the oncology model with total integration between clinical practice and research. The next step is to improve integration and to close the gaps between research and education as well as between mainstream oncology and palliative care research. From a palliative care perspective, the field needs to reach a certain level of research competence in order to be an interesting collaborator for oncology research.
In 2009, the European Palliative Care Research Centre (PRC) was established in Trondheim as a partnership among the Trondheim University Hospital, the Norwegian University of Science and Technology (NTNU), and the Norwegian Cancer Society (35, 36). The PRC is having a major international outreach with key collaborators from 15 international (from Europe, North America, and Australia) and 7 Norwegian institutions being successful as measured by 142 publications being published in international peer-reviewed journals during the last 5 years. In addition, a close collaboration with INT in Milan has existed since before the establishment of the PRC and has been further developed in recent years. The PRC aims at improving palliative care through research, education, and implementation of research findings in an international setting. The research priority for the next 5-year period is to intensify and deepen research on host‐ and tumor-related factors in patients with cancer with a primary focus on pain, cachexia, and central nervous system effects.
This collaborative model of clinical research in palliative care is outlined in
Oncology and palliative care: clinical research collaboration.
Challenges and solutions for the future
In order to reach the overall goal of practicing evidence-based medicine in both palliative care and oncology, robust systems for formal and informal collaboration in clinical practice and research are needed. A (standardized) care pathway is defined by the European Pathway Association as “a complex intervention for the mutual decision making and organization of care processes for a well-defined group of patients during a well-defined period” (40). This is a method that can be applied to implement results from research into patient-centered care (
Standardized care pathway as a method for implementation of research results into clinical practice.
The key challenge is to develop standardized care pathways detailed enough so that the patient flow can be planned according to the needs of each individual patient. In other words, the standardized care pathways need to be sufficiently detailed but also flexible in order to address individual needs. By including the integration goal with the planning methodology, i.e., standardized care pathways for oncology patients at any stage, the WHO goal of optimal QoL for the patients can be reached.
The integrated model between community healthcare and specialized healthcare at local and university hospitals (
Challenges of a total integration model between oncology and palliative care
|Reimbursement: 2 levels of economy|
|Budgets for primary and specialized care separate|
|Professionals hired by different bodies|
|Oncologist: competence in palliative care|
|Palliative medicine: competence in oncology|
|Competence of palliative care and oncology care in community health care level is limited|
|Curative, life-prolonging, and palliative care in the same clinics|
|Volume of palliative care in community health care specifically for the general practitioners (0-3 patients per year)|
|Level and amount of availability from the hospital palliative care team to home care is limited|
Symptom management is essential in oncology for curative, life-prolonging, and palliative treatment intentions. It has been recommended to routinely assess and screen for symptoms in cancer care. Until recently, if performed, paper and pencil methods were applied (42). The introduction of modern information technology software and hardware has given the possibility for new solutions for computer-based assessments of symptoms and functions.
At the European Palliative Care Research Centre, NTNU, we have developed new interactive software called EIR for symptoms assessment. In this system, used on an iPad or similar device, the patient completes the symptom assessment. First a symptom screening is performed based on the screening (stage 1) and thereafter more detailed questions are completed, custom-selected for each individual patient (stage 2). This gives a more detailed classification and information about symptoms and conditions such as depression, cancer pain, cancer neuropathic pain, and cancer cachexia. Then the data are wirelessly transferred (stage 3) to the working station of the physician where the symptom profile is presented and where advice for treatment and interaction may be given (
Examples from the EIR computer-based assessment and decision-making system. (
What are the potential benefits to patients, families, and society?
The overall aim of palliative care in cancer care is to improve patients’ QoL. The approach is patient-focused and not focused on the tumor, but on the consequences to the patient caused by the tumor from metastatic or local regional disease. The palliative care approach is symptom- and function-oriented. Physical, mental, social, and spiritual functions are to be addressed and intervened upon according to the patients’ needs.
By combining the structure of the standardized care pathway, the symptom assessment software EIR, and the basic structure of the organization in our healthcare system, better patient-centered care can be achieved in oncology. The main challenges are probably to change healthcare providers’ attitudes and behaviors. However, these models of care that can be considered to be more patient-centered will probably be more cost-effective and give better resource allocation and higher level of patient and family satisfaction.
Patients and families today are expecting a total care approach independent of the treatment intention being curative, life-prolonging, palliative, or end-of-life care. The competence of oncology—with basic and clinical knowledge on how to treat the tumor and care for the patients—and the palliative care approach with specialist skills and knowledge of symptom assessment and management, psychosocial and spiritual issues, as well as expertise in coordination of the care processes will, if well-integrated, planned, and conducted, have the potential to offer optimal cancer care. Standardized care pathways may be used as a method for optimal patient-centered planning. Patients are often asking what is happening to them, what the plan is, and who is caring for them. Optimal standardized care pathways can be given to the patients as individual plans with clear definitions of who is doing what at any given point in time. This also includes a clarification of how oncologists and palliative care physicians work together at any time during the care trajectory.
It is impossible to know whether the Milan trio—Bonadonna, Veronesi, and Ventafridda—would have agreed with the approach of total integration of medical oncology, radiation oncology, palliative medicine, and surgical oncology. They may have agreed to make common plans for clinical care, and they may have identified areas of care that need improvements. They probably would have agreed upon common research proposals in the name of better QoL for all patients.
The authors thank Gitte Tvetenstrand Korman, Oslo University Hospital, Oslo, Norway, for organizational help and preparation of the manuscript.
- Kaasa, Stein [PubMed] [Google Scholar] 1, 2, 3
- Knudsen, Anne Kari [PubMed] [Google Scholar] 1, 3
- Lundeby, Tonje [PubMed] [Google Scholar] 1, 3, * Corresponding Author (firstname.lastname@example.org)
- Loge, Jon Håvard [PubMed] [Google Scholar] 1, 2, 3
Department of Oncology, Oslo University Hospital, Oslo - Norway
Medical Faculty, University of Oslo, Oslo - Norway
European Palliative Care Research Centre, Department of Cancer Research and Molecular Medicine, NTNU, Trondheim - Norway