Support Care Cancer DOI 10.1007/s00520-015-2961-9

ORIGINAL ARTICLE

Supportive/palliative care in cancer patients: quo vadis? Jean Klastersky 1 & Isabelle Libert 1 & Bénédicte Michel 1 & Myriam Obiols 1 & Dominique Lossignol 1

Received: 4 August 2015 / Accepted: 14 September 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract Supportive care in cancer has become a paradigm for the treatment in oncology. Now, we have guidelines and active research in that field, making this area of clinical oncology both authoritative and rapidly progressing.The present paper focuses on the clinical experience of a group involved with supportive care in cancer patients for more than 25 years; it is hoped that our considerations might be helpful for further developments in this concept.

Keywords Palliative care . Early palliative care . Best supportive care

Introduction: historical perspective Supportive care in cancer patients has appeared at the same time as effective medical therapy for neoplastic diseases. In the early 1960s, chemotherapy started to be used routinely for the treatment of acute leukemia; as a consequence, bleeding due to thrombocytopenia and infection due to granulocytopenia became the nightmares of the clinicians trying to bring their patients into remission. Platelet transfusion and empirical antimicrobial therapy for febrile neutropenia are the first examples of supportive care that improved the quality of life and survival of chemotherapy-treated patients.

* Jean Klastersky [email protected] 1

Medicine Department, Supportive Care Unit, Institut Jules Bordet, Université Libre de Bruxelles, Rue Héger-Bordet 1, 1000 Bruxelles, Belgium

Over the next years, the treatment of cancer with chemotherapy was progressively extended to patients with solid tumors. This evolution made it necessary to address non-hematological toxicities as well. Namely, the control of nausea and vomiting made cisplatin and other highly emetogenic regimens acceptable. At the same time, as advanced cancer progressively became a more chronic disease, and the focus on the patient’s well-being and overall quality of life steadily increased. In this respect, major milestones were achieved, namely adequate control of chronic pain and development of appropriate psycho-social care, as well as attention to various ethical issues, including the specific aspects related to the end of life [1, 2]. This historical perspective needs necessarily to deal with certain semantic aspects of the terms used with respect to the care for the well-being of cancer patients; these concepts have been recently reviewed [3]. Suffice it to say that it is the term Bpalliative^ which complicates several issues here. Palliative means, stricto sensu, a measure that helps a patient but will not cure him from the disease; in that sense, most of what medical oncologists do today is palliative care! Of course, this is not what is meant when we use the term Bpalliative care^ today. Actually, palliative care has become a surrogate for terminal care; i.e., the type of approaches which are indicated and needed during the last weeks of life in patients with ultimately lethal chronic diseases. The issue is further complicated by the concept of Bearly palliative care^, which has been introduced recently and which will be discussed later [4]; here, we are dealing with a psycho-social support of patients with advanced cancer aiming at improving the patient’s information in order to increase his autonomy with respect to major decisions regarding palliative (in the true sense of the word) cancer treatment decisions.

Support Care Cancer

Thus, we have to accept and live with these contradictory and potentially misleading definitions; probably, the safest way around it is to clearly define what is meant when the Bpalliative^ term is used [5]. Finally, from an historical point of view, it should be stressed that supportive care in cancer patients has become a medical specialty of its own. It started as the genuine intent of the oncologist to meet the side effects and consequences of aggressive cancer treatment; today, it is a complex discipline encompassing multiple medical approaches and involving many different medical and paramedical competences [6]. Although unifying efforts have been made in that field, such as the creation of Multinational Association for Supportive Care in Cancer (MASCC) and the foundation of the Journal of Supportive Care in Cancer, it remains that supportive care is a heterogeneous area with a variety of interests and a multiplicity of actors [7]. Nonetheless, it remains a unifying concept in order to organize a comprehensive spectrum of multidisciplinary expertise around the cancer patient, covering all necessary aspects of support in conjunction with specific anti-cancer therapy. It also stresses the educational ambitions and the need for progresses through structured research and communication.

Supportive care as a comprehensive approach When the concept of supportive care was initially formalized [5, 6], it was proposed as a comprehensive Bumbrella^ aimed to cover all the needs of cancer patients (in addition to the specific oncological management) in order to provide an optimal quality of life. At that time, it was already clear that supportive care addressed all the stages of cancer: curative and palliative treatments as well as terminal care; this latter soon became palliative care on its own, as already mentioned. This comprehensive spectrum of supportive care, illustrated in Fig. 1, is still accepted today, as stressed in a very recent review [5], with some changes and improvements that will be discussed later. In order to fully grasp the concept of supportive care, it is particularly important to understand that palliative care (or terminal care) remains a part—clearly an essential one—of supportive care, which should be viewed as the internal and psycho-social medicine that applies to the cancer patient throughout the disease [8]. Should supportive care be further defined? This is an important issue for several reasons. Firstly, considering supportive care as a kind of general Bbest supportive care^ is not acceptable because best supportive care is inadequately described in studies using that terminology [9]. Moreover, it is an ethical obligation towards the cancer patient starting any therapy to provide him with comprehensive information about all aspects of what the oncological and supportive therapy will consist of; this is particularly important if a specific

Fig. 1 Comprehensive spectrum of supportive care

oncological therapy becomes less effective or if the patient accepts to be enrolled in clinical studies with a no-treatment option. How far should we go in the definition of supportive care? Based on the preceding considerations, it appears that a patient, undergoing oncological therapy, in a curative or palliative (strict definition) setting, should be fully informed not only about the expectations of specific anti-cancer treatment but also about the possibilities available to palliate the adverse effect on oncological treatments and, more generally, to secure on optimal quality of life. The same type of information needs to be provided, mutatis mutandis, to patients with terminal illnesses. As indicated in Table 1, there is a wide variety of expertise that should be available; this list is neither exhaustive nor definitive, as supportive care, just as other medical areas, remains in a constant stage of evolution [10]. It is not within the scope of this review to examine in details the different areas which constitute supportive care today; comprehensive textbooks are available and can be referred to [1, 2]. The only area which deserves a special comment is the concept of early palliative care, as proposed by Temel et al. [4].

Early palliative care Although the concept of early palliative care is innovative and timely, the terminology just adds to the general confusion, as already mentioned; probably a more appropriate appellation might have been Bpsychosocial support for cancer patients treated with a palliative intent^, while the early palliative care has a connotation of Bearly^ or Bpre^ terminal care, what it is actually not. On the other hand, one could imagine that once cancer is diagnosed as Bnot curable^—and here the definition of curable

Support Care Cancer Table 1 A wide variety of expertise that should be available in order to provide adequate supportive care Areas in which expertise should be available in order to provide adequate supportive care Anemia Bleeding Nausea and vomiting Diarrhea Nutritional support Pain management Obstructive syndromes Malignant effusions Oral mucositis Stoma care Intravenous access Intensive care Central nervous system metastases Skeletal metastases Venous thrombo-embolism Psycho-social and ethical issues Sexual function Multicultural dimension Early palliative care Adapted from reference [10]

cancer remains a source of controversy and an area for further research [11]—one has to envision the worst outcome and get the patient prepared for it. In that concept, it would make sense that an early-palliative-care phase prepares the patient for the consequences of a dismal course of the disease which will sooner or later lead to the palliative care or Bterminal^ care or Bend of life care^ (see Fig. 2). The concept of early palliative care probably stems from the need to better inform the patient with non-curable cancer about the real possibilities of the available treatments and avoid over treatment which might interfere with the preservation of an optimal well-being. Clearly, many patients with advanced cancer still believe that palliative cancer treatment might significantly prolong their lives or even cure them [12]. This misunderstanding is due to both patients and oncologists, as already stated, and definitely needs measures to be avoided. The concept of early palliative care goes into that direction. As stated by Temel et al. [4] in their prospective randomized study of early palliative care, a specific attention was paid to assessing physical and psycho-social symptoms, establishing goals of care, and coordinating care on the basis of the individual needs of the patients, who all continued to receive routine oncologic care (specific cancer therapy and general supportive care) throughout the study period. This novel concept implies multidisciplinarity for its implementation; as we already suspected, many years ago, [6, 7] supportive care

progressively has evolved beyond the field of practicing oncologists and now requires specialists involved in many different fields. As recently stressed by Hui [5], primary care (oncological and supportive) is provided by oncologists and primary care teams who provide management and information in the frontline setting; secondary supportive care (palliative care) is provided by teams with specialized expertise such as terminal care, wound care, psychiatric, and pain control on a consultation basis. As already mentioned, the patients who benefited from the early palliative approach (as described in Temel’s study) had a better quality of life and lived actually longer than those who received standard care only [4]. Since then, two other studies supported the early introduction of palliative care, i.e., psycho-social support, into the management of cancer patients, once the disease is no longer curable [13, 14]. At that point, it is important to weight the aggressiveness of the cancer treatment against its expected benefits and to tailor it to a minimal risk of complications in order not to require vigorous supportive care and prolonged hospitalizations. Studies to develop guidelines to assist in the de-escalation of inappropriate medications in those patients are urgently needed [15]. Realistic awareness of the prognosis is mandatory to achieve these goals and requires assistance by expert qualified personnel; this communication between the patients and caregivers involves many ethical issues and requires special expertise [16]. An important but delicate issue here is the more or less close, but definitely perceivable, lethal issue of the disease. In the mid-twentieth century, Bthe process of death and dying was twice removed and rendered invisible, one through hospitalization and then through ICU^ [17]. The right for refusal of ICU and resuscitation should be granted to patients through optimal communication. However, the problem is not only where to die but maybe more importantly how to die. Several options are available here, including hospice care, optimal pain palliation, sedation for intolerable suffering, assisted suicide, and euthanasia. At what time these questions should be raised and by whom is unsettled so far and depends on legal and cultural issues. It remains necessary to implement an expert communication between the caregivers and the patients in a near future as more and more patients seek information on the Internet about their disease and all the aspects associated with it, including the difficult aspects of the end of life [18, 19].

The extremes of supportive care Today, there is a clear indication that we are curing an increasing proportion of patients with cancer; moreover, the economic and social consequences of converting cancer into a curable or chronic disease are considerable [20]. Two hundred years

Support Care Cancer Fig. 2 An early-palliative-care phase prepares the patient for the consequences of a dismal course of the disease which will sooner or later lead to the palliative care or Bterminal^ care or Bend of life care^

Curable disease

Not curable

Terminal disease

Oncological care

Supporve care Follow-up of cured paents

Palliave care

Early palliave care

End of life care

Berea vement for families and care givers

Oncologist

Supporve/palliave acve team Palliave care specialists Cancer treatment for cure or palliaon

of cancer research are starting to produce significant benefits. It remains, nonetheless, that a substantial proportion of those who are cured from cancer, especially the patients who required radiotherapy or/and chemotherapy, will experience, over the following years, an impressive series of complications, among which the occurrence of second malignant neoplasm is one of the most common ones and carries the worst prognosis [21]. The vast and varied list of possible complications after chemoradiotherapy in patients cured of cancer requires a special attention during a careful follow-up. Sequelae such as metabolic syndrome, growth deficiency, sexual dysfunction [22], neurocognitive deficits, and many other aspects require specific measures to permit optimal social adjustment, as the awareness of possible sequelae represents a psychological burden for those patients who are cured [23], in addition to the always present fear of late relapse. It should be stressed that complications, some of which are potentially fatal, continue to occur 20 to 30 years after treatment; this requires prolonged follow-up, necessarily associated to psychological stress [24]. There is obviously a new avenue here for supportive care (maybe it should be renamed Blate palliative care^) for those patients who are cured of cancer. These new approaches will require special expertise taking into account the everyday

Basic supporve care acute complicaon

Chronic symptoms management

Psychosocial guidance

Comfort symptoms management

Assistance with dying

Bnormal^ life of patients who went through the burden of a diagnosis of a potentially lethal disease and through a demanding therapy that eventually led to a cure, shadowed by the risk of second malignancies and/or late appearing of morbid consequences. The other extreme of supportive care is the bereavement following the patient’s death. At a time, when dying at home, surrendered by supportive relatives, was the standard, death was part of life, and its acceptance was made more tolerable by the social (and religious) environment. Now, as more than half of the deaths in our countries occur in hospitals, namely in ICUs, dying has become less socially personalized and can be lived as a failure of modern medicine [25]. As a consequence, the bereavement process may be disrupted and prolonged. Families of patients with cancer, especially if the disease had a prolonged course, might adapt better to the fatal outcome, namely if there has been a satisfaction with the provided care and if the psycho-social support of the patients and the relatives has been satisfactory. Nonetheless, the expectations for cure or prolonged palliation are increasing today and may lead to poor acceptation of the fatal outcome by relatives, if no adequate support is provided prior and after the patient’s death. It has been shown that family members of patients who experienced spiritual and psychological distress were

Support Care Cancer

more likely to have an extended and complicated grief and bereavement process and were at higher risk for illness and death [26]. Providing psycho-social, spiritual, and bereavement support to caregivers is also a key component of late palliative care. Support groups have been found to reduce stress and depression experienced by caregivers [27]; such programs should be implemented in all units treating seriously ill patients during their end-of-life period and caring for their families, in order to minimize the feeling of failure among caregivers, leading to loss of self-confidence and burn-out [28].

Practical aspects of supportive palliative care As already mentioned, supportive care for cancer patients is clearly a multidisciplinary undertaking, which is providing to the clinical oncologist the comprehensive approach to insure optimal quality of life for the patients at all stages of the disease [5]. Clinical oncologists should not only be experts in cancer therapy but should also be competent with basic supportive care aimed at the control of acute complications, such as infection, nausea and vomiting, pain, cancer-related metabolic and ionic disorders, and the continuously enlarging spectrum of complications related to newly introduced targeted biological cancer therapy. The oncologist should be aware of what each patient needs in addition to oncological expertise and should consequently resort to the support of an active supportive/palliative team having expertise in the management of many chronic and/or recurrent symptoms such as pain, malnutrition, obstructive syndromes, psychiatric, and neurological disorders to cite only the most common ones. The interventions by these experts become essential, once the patient is no longer a candidate for the cure. It is important that the early palliative care team starts to provide psychosocial guidance to ensure optimal patient’s autonomy and continues to do so throughout the rest of the patient’s life, especially when specific oncological care becomes futile. At that point, in full interaction with the patient, the discussion of how life might be ended becomes an important part of palliative care [29, 30]. Palliative care specialists (e.g., those implementing the hospice philosophy) will take over when the patient’s life expectancy is short and when the only priority of care is pain control and psychological well-being of the patient and of his relatives. This ideal organization of supportive/palliative care requires frequent and constructive communication between all teams (Fig. 3); it also needs coordination as well as geographical unity coupled with mobility. The concept of supportive/palliative care, based on our experience at the Institute Jules Bordet, postulates that it is the oncologist who should coordinate not only the treatment

PALLIATIVE CARE = supporve care aimed at the opmal well-being and maximal autonomy of the paent with advanced cancer

EARLY PALLIATIVE CARE Psycho-social care for the not curable cancer paent sll receiving an-cancer therapy to help with maintaining realisc informaon and adequate decision making regarding connuaon of therapy

END OF LIFE CARE Comprehensive care for the paents not receiving ancancer therapy and considered to be near to the end of life in order to provide opmal well being to the paents and relaves

Fig. 3 Ideal organization of supportive/palliative care

of cancer but all the other phases that go with it. The oncologist, who has the closest relationship with the patients, has to work in relationship with the supportive/ palliative active team. Even if cancer therapy becomes futile and namely when a very short survival is expected, ideally the oncologist should still remain in some kind of contact with the patients; this obviously requires geographical unity. The concept of a supportive/palliative active team refers to a service aimed to preserve the physical and psychological well-being of the patient once cancer therapy is no longer curative and as long as death is not imminent. That team should consist of physicians with expertise in pain control, other various chronic complications, and psycho-social support; they should benefit from the close support of psychologists, nurses, social workers, nutritionists, physiotherapists, ostomy care, etc. The active supportive palliative team ideally assumes a triple role: it is available for consultations aimed to hospitalized patients, it provides out-patient contacts and finally, and it runs a limited in-patient unit (at the Institute Bordet, there is a 12-bed unit for that purpose, the total capacity for hospitalization being 150 beds) for admission of patients with acutization of chronic symptoms (pain, obstruction, depression, malnutrition, etc.) with the ultimate goal of improving the patient, morbid manifestations, and discharging him back home or the place he used to live; sometimes, the patient can be oriented to a palliative care unit. In many places, including ours, the real palliative care units (hospices) are located outside the cancer center. This is unfortunately not the optimal way to ensure the continuity of care from possible cure to end of life and allow the oncologist to remain the coordinating element of the patient’s course. Nonetheless, this is the way how situations evolved over the last years, at least in our hospital; it will be interesting to evaluate, in the future, the patient’s well-being in more geographically concentrated approaches.

Support Care Cancer

Conclusions This review is not intended to be a comprehensive review of the literature dealing with supportive/palliative care. It is instead an attempt to critically review the current practice in that field and suggest some possible avenues for the future, based on extensive experienced accumulated in our center. In our view, and beyond the semantics, supportive care should be reviewed as a comprehensive complement to oncological care, aiming at an optimal physical and psycho-social well-being of the patient. It includes 3 main stages: the control of acute complications of cancer and/or its therapy; the management of pain and chronic complications as well as psychosocial support once oncological therapy is no longer curative and, finally, the approach of the end of life. These 3 phases have, and should have, overlapping areas; this requires communication and understanding among caregivers, as well as coordination, ideally by the oncologist. In addition, supportive care should include, on one hand, the prolonged follow-up of patients cured of cancer, and, on the other hand, the bereavement for relatives and caregivers. It should also be stressed that our concepts and paradigms are in a constant stage of evolution and that we need to constantly adapt to the progresses of medicine. The role of research and education cannot be overemphasized. Acknowledgements The skillful secretarial help of Marie-Aline Echterbille and Nadia Santoro was fully acknowledged. Conflicts of interest The authors declare that they have no competing interests.

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