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Prognostic Factors in Advanced Cancer Patients: Evidence-Based Clinical Recommendations—A Study by the Steering Committee of the European Association for Palliative Care

From the Palliative Care Unit, Department of Medical Oncology, Morgagni-Pierantoni Hospital, Forlì; Istituto Scientifico Romagnolo per lo Studio e Cura dei Tumori, Forlì-Meldola; Palliative Care Unit, National Cancer Institute, Milan, Italy; Faculty of Theology, Catholic University, Leuven, Belgium; Department of Health Care Policy, Harvard Medical School, Boston, MA; Department of Palliative Care, Kantonsspital, St Gallen, Switzerland; Department of Palliative Care, Royal Prince Alfred Hospital, Sidney, Australia; Hospital Universitario Arnau de Vilanova, Valencia, Spain; Palliative Care Division, McGill University, Montreal, Quebec, Canada; Centre for Nursing Studies, National University of Ireland, Galway, Ireland; Department of Palliative Medicine, University of Bristol, Bristol Hematology and Oncology Centre, Bristol, United Kingdom; and Department of Oncology and Radiotherapy, Trondheim University Hospital, Trondheim, Norway

Address reprint requests to Marco Maltoni, MD, Palliative Care Unit, Department of Medical Oncology, Morgagni-Pierantoni Hospital, Via Forlanini, 34, 47100 Forlì, Italy; e-mail: ma.maltoni{at}ausl.fo.it

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION Appendix Authors' Disclosures of... REFERENCES

 
PURPOSE: To offer evidence-based clinical recommendations concerning prognosis in advanced cancer patients.

METHODS: A Working Group of the Research Network of the European Association for Palliative Care identified clinically significant topics, reviewed the studies, and assigned the level of evidence. A formal meta-analysis was not feasible because of the heterogeneity of published studies and the lack of minimal standards in reporting results. A systematic electronic literature search within the main available medical literature databases was performed for each of the following four areas identified: clinical prediction of survival (CPS), biologic factors, clinical signs and symptoms and psychosocial variables, and prognostic scores. Only studies on patients with advanced cancer and survival 90 days were included.

RESULTS: A total of 38 studies were evaluated. Level A evidence-based recommendations of prognostic correlation could be formulated for CPS (albeit with a series of limitations of which clinicians must be aware) and prognostic scores. Recommendations on the use of other prognostic factors, such as performance status, symptoms associated with cancer anorexia-cachexia syndrome (weight loss, anorexia, dysphagia, and xerostomia), dyspnea, delirium, and some biologic factors (leukocytosis, lymphocytopenia, and C-reactive protein), reached level B.

CONCLUSION: Prognostication of life expectancy is a significant clinical commitment for clinicians involved in oncology and palliative care. More accurate prognostication is feasible and can be achieved by combining clinical experience and evidence from the literature. Using and communicating prognostic information should be part of a multidisciplinary palliative care approach.

	INTRODUCTION

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Besides being one of the core skills in the practice of medicine,^1,2 prognostication in advanced cancer has special importance. In advanced phases of the disease, prognostication cannot be based on the same information as in earlier stages, when it is typically based on tumor stage.^3-5 However, accurate prediction of survival is still necessary for clinical, organizational, and ethical reasons, especially in helping to avoid harm, discomfort, and inappropriate therapies in vulnerable patients⁶ and, conversely, in planning specific care strategies. Additionally, important personal decisions are influenced by prognostic information, and therefore, patients' autonomy can be enhanced by providing better prognostication within the context of appropriate communication.^7-9

Prognostic accuracy in this population seems to be the exception rather than the rule. A large prospective cohort study, involving 343 doctors and 468 hospice outpatients, found that only 20% of prognoses were accurate and that, overall, doctors overestimated survival by a factor of approximately 5.¹⁰ Therefore, the Research Network of the European Association for Palliative Care decided to establish a Working Group (WG) with the aim of providing evidence-based recommendations on the use of prognostic factors to determine length of survival in advanced cancer patients.

	METHODS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION Appendix Authors' Disclosures of... REFERENCES

 
The WG reviewed several sources describing the clinical guidelines development process,^11-14 and the following steps were adopted: (1) defining group membership; (2) identifying the target population; (3) defining the key questions; (4) systematically searching the literature; (5) assigning the level of evidence to the selected literature; and (6) formulating and grading the final recommendations.

Defining Group Membership
WG members were identified on the basis of their clinical experience in palliative care and in prognostic cancer studies (M.M., A.C., N.C., S.E., P.G., M.N., and A.V.). Members with epidemiologic and statistical expertise were also enlisted (C.B., P.G., and A.V.), and the contribution of an experienced nursing person was ensured (P.L.). Practical and ethical considerations determined the exclusion of patients. Sociologic and philosophical points of view were available (B.B. and N.C.). Finally, the group conclusions were submitted to external reviewers (F.D.C., G.H., and S.K.) and to the Steering Committee of the European Association for Palliative Care Research Network.

Identifying the Target Population
Accepted criteria for staging advanced cancer patients are lacking. Some authors have attempted to describe, with subjective criteria, inception cohorts,^15-19 whereas others have examined patient populations referred to a palliative care program.^20,21 However, many studies have shown that the median survival in populations of advanced cancer patients undergoing palliative care is less than 90 days.^15,22-24 For these reasons, only populations homogeneous by survival (survival cohort)²⁵ were included by selecting studies in which the median survival of the group was 90 days, excluding surgical series.

Defining the Key Questions
The WG defined six key questions, which developed into recommendations, that were assigned to different pairs of group members to carry out a literature search and analyze the available evidence about the usefulness of an accurate prognostication of life expectancy in advanced cancer patients, the prognostic role of clinical signs and symptoms, psychosocial characteristics, laboratory parameters, and prognostic scores.

Systematic Literature Search
Systematic reviews were performed for each area of interest. The search for relevant articles was performed on the Medline and Embase databases. The search strategy is presented in Table 1. A hand search of the References section of electronically identified articles was also performed. Articles not based on original data (unless formal meta-analyses) were excluded.

Assigning the Level of Evidence to the Selected Literature
The level of evidence attributed to the results from each study was based on the methodologic quality of the study and on the study type.^11-13 A quality assessment checklist, based on the existing literature,^12,28-35 was formulated (Table 2). When evaluating meta-analyses, homogeneity of results was required to ensure quality. The study type classifications are listed in Table 3. ^12,29,31 Quality and study type classification levels were combined to give the final level of evidence (Table 4, modified from the Centre for Evidence Based Medicine Web site).¹² Each study was evaluated independently by at least two group members.

	RESULTS

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The literature review produced a list of publications, which are listed in Table 5, that show the quality and characteristics of the evidence that was used to formulate the following recommendations (listed in brief in Table 6).

There is no study on prognostic factors aimed at evaluating whether an accurate prediction of survival can improve actual clinical care; that is, there is no impact study concerning the role of prognostic tools in improving decision making in the palliative care of advanced cancer. Despite this, it is the opinion of the WG that increased prognostic accuracy would assist health professionals to improve their care strategy and help patients and families to make more informed choices.^10,22,23,65

Recommendation 2. The Clinical Prediction of Survival (CPS) is a generally useful and valid tool but is subject to a series of factors that limit its accuracy. The CPS should not be used alone but in conjunction with other prognostic factors (grade A).

CPS could be defined as clinical prognostic judgment; it is subjective and depends on the clinician's assessment of the individual patient at the bedside or in the clinic. The prognostic value of CPS has received a great deal of criticism in the literature because of the characteristics previously mentioned and because of its inherent nonreproducibility.

Our systematic review of the literature on CPS resulted in the selection of 27 articles, 11 of which were excluded. In the 16 eligible studies,^{10,15,16,18,20,36-46} the correlation coefficient of CPS/actual survival varied between 0.2 and 0.65. In all the studies examined in a review published in 2000, CPS was reported as having an independent effect when used with most other prognostic factors or tools.⁵ When using CPS, physicians need to be aware that it is subject to a series of features and shortcomings that limit its prognostic capacity. CPS is more than twice as likely to be overoptimistic versus overpessimistic and to overestimate the length of actual survival by a factor of between 3 and 5 (grade A).²⁶ CPS is subject to the Horizon Effect^24,66,67 (grade B), which is a term taken from the language of weather forecasting and used in clinical prognostication to mean the greater accuracy of short-term predictions over long-term predictions. Therefore, repeated evaluations of CPS at fixed intervals may be opportune (grade A). Considering CPS as a probability rather than a temporal value would ensure a greater accuracy (grade A). Lack of experience in oncology and palliative care reduces accuracy, and thus, a second opinion by a more experienced professional could be useful (grade D). A second opinion could also be worth obtaining if the first physician has a close relationship with the patient (grade B).

Clinicians should consider using CPS in combination with other prognostic factors or scores to improve the accuracy of their predictions (grade A). Training in prognostication could improve the accuracy of CPS (grade D).

Recommendation 3. Certain clinical signs and symptoms have proven to be prognostically significant in this patient population, the most important of which are performance status (grade B), some symptoms of the cancer anorexia-cachexia syndrome (CACS; grade B), dyspnea (grade B), and delirium or cognitive failure (grade B). Factors linked to the patient or to the primary/metastatic site and biologic characterization of the tumor do not seem to be prognostically important in advanced cancer, as defined in this review.^{15,16,18,47-50} Conversely, a correlation between some clinical signs and symptoms and survival has been confirmed in numerous multivariate analyses. In this section, of the 80 works analyzed, the 20 studies considered^{15,16,18,20,37,40,47-60} show that performance status^{18,37,40,47,51,52,54,57,59} and various indices of activity and functional autonomy^{15,16,49,50,53,55} are prognostically significant. In particular, low performance status is considered a reliable prognostic factor to predict short-term survival. However, initially high scores are not necessarily predictive of a long survival, whereas their deterioration often indicates a serious worsening of the prognosis.^{18,20-22,40,42,47,51-56}

Signs and symptoms characterizing a clinical condition that is often termed the common terminal pathway,^54,69,70 including nutritional status and CACS, anorexia,^{18,21,53,54,56} weight loss,^{17,18,20,52,57} dysphagia and difficulty in swallowing,^18,20,21,52 and xerostomia,^18,20,52,56 have a prognostic impact. Finally, there is significant evidence of the prognostic importance of dyspnea^{18,48-50,52,57} and delirium or cognitive impairment.^{20,47,57,58,60}

Other signs and symptoms (nausea, constipation, dizziness, anxiety, depression, fever, pain, diarrhea, hemorrhage, pulse, and respiratory rate), polymorbidity, opioid therapy, and therapeutic and diagnostic interventions^{18,20,47,50,52,54,59} have occasionally proven to be significant, mainly in less advanced stages of the disease. However, these symptoms have not been confirmed in multivariate analysis, especially in the far advanced patient population.

The prognostic capacity of subjective indicators of quality of life or other psychological parameters is somewhat contradictory. Although they are certainly relevant in the earlier stages of disease,^71-78 the prognostic relevance of multidimensional tools in patient populations with a median survival of 90 days or less seems to be attributable to the physical-symptomatic component of the test.^15,56

Recommendation 4. There is some evidence that abnormalities in certain laboratory tests (particularly leukocytosis, lymphocytopenia, and elevated C-reactive protein) have prognostic significance (grade B). The need for a blood sample also needs to be weighed against the likely clinical advantage for the individual patient (grade D). Biologic parameters have not been as widely investigated as clinical parameters in this population of patients,⁵ and a more accurate evaluation of these variables in relation to prognosis is undoubtedly warranted.

In the present review, a total of 23 biologic factors were studied in the nine works^{16,42,47,54,59,61-64} selected for assessment. Laboratory parameters that proved significant in at least one multivariate analysis were low pseudocholinesterase,⁶¹ high vitamin B₁₂,⁶³ and high bilirubin.⁵⁴ Statistical significance in more than one study was observed for elevated C-reactive protein,^63,64 lymphocytopenia,^42,61 and leukocytosis.^42,61 The same biologic parameters also proved to be prognostically valid in other heterogeneous populations of patients with less advanced disease. This positive relationship was, conversely, lost by some factors, such as low serum albumin, in the patient population evaluated in the present study. For some factors, such as albumin and prealbumin levels, this could be attributed to a close correlation with other CACS characteristics that maintain their significance, to the detriment of weaker factors.

Recommendation 5. A number of prognostic scores or indices have been developed that are easy to use and permit a rapid estimate of life expectancy by placing patients into broad groups that differ significantly in survival (grade A). Some authors have built and validated prognostic scores for patients in palliative care programs. These scores are constructed on the basis of prognostic factors that have proven to be significant in multivariate analysis and have been validated quantitatively on the basis of their individual prognostic weight.

Only eight of the 24 studies identified satisfied the review requirements. Of these studies, four involved construction and development of scores,^19-21,42 whereas four concerned the validation of two of the scores, the Palliative Prognostic (PaP) Score and the Palliative Prognostic Index (PPI).^43,44,58,62 The PaP Score (Table 7) was built and validated in two independent multicenter population studies and is the only measure to include some simple biologic factors that require a blood sample. It has been validated in several countries, in various settings, and in different disease phases.^{23,42,43,58,62} This score includes CPS, which means that it is used together with, rather than instead of, clinical judgment. The PaP Score was not constructed to include hematologic malignancies and, therefore, cannot be used in this patient population. Furthermore, the score does not include delirium, which was subsequently demonstrated to subdivide each population categorized by the PaP Score into two further prognostic subgroups.⁵⁸

Recommendation 6. Establishing an accurate prognosis is part of the therapeutic alliance. Patients have a right to be informed of their prognosis or, if they prefer, not to be informed. Using and communicating prognostic information should be within the context of a comprehensive, individualized, patient-centered approach (grade D).

A number of principles should be applied to this clinical situation. First, do not be a burden to the patient. From an ethical point of view, it is important that prognostic tools do not impose an additional burden on the patient, be it directly or indirectly (ie, by being time consuming and, thus, leaving less time for other aspects of patient care).

Second, use prognostic information within an ethically valid approach. It is important to understand that a prognosis is established, used, and communicated. Although our recommendations concentrate on establishing a prognosis, we should not forget that, once established, a prognosis should be used in an appropriate way. Treatment decisions should be based on a number of variables, including prognosis, and all these variables should receive due attention. The fact that prognostic information is, by definition, probabilistic, and that even the best prognostication will be dramatically inaccurate for a significant number of patients provides an additional reason for never losing sight of the patient and his or her individual trajectory and personal history. Prognostication that is not deeply embedded in an open, flexible, patient-centered, and dialogic approach is potentially dangerous.

Third, communicate prognosis when requested and in an appropriate way. Patients have a right to be informed about their prognosis, but they also have the right to refuse to be informed. When prognosis is communicated, ethical, cultural, religious, and psychological considerations are of fundamental importance to avoid inflicting additional harm to the patient.

Fourth, place emphasis on a holistic therapeutic approach beyond time limits. It is only by working within the realms of multidisciplinary palliative care and by continuing to consider the individual value of the patient's residual life that life expectancy prognostication can improve and further personalize the care of advanced cancer patients.

	DISCUSSION

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The recommendations made here are confined to a population of patients with advanced cancer and a median survival of no more than 90 days. The WG demonstrated that, given the available literature evidence, prognostication of life expectancy in advanced cancer patients is feasible and facilitated by the use of clinical tools such as signs and symptoms, laboratory examinations, and prognostic scores. In particular, strong evidence of prognostic significance has emerged for CPS, performance status, clinical symptoms of CACS (anorexia, weight loss, dysphagia, and xerostomia), dyspnea, delirium, some biologic factors (leukocytosis, lymphocytopenia, and C-reactive protein level), and prognostic scores (Table 8).

It is important to point out that prognostic information should not be limited to palliative care populations, but it can also be used to gain a better understanding of patient survival before referral for palliative care. More studies on well-defined inception cohorts are needed to improve our knowledge in this field.

Finally, it is clear to the WG that ethical considerations regarding prognostication at the end of life are indeed of fundamental importance. The failure to prognosticate or to prognosticate accurately can, in some circumstances, be as harmful as a mistaken diagnosis or therapy. The fallibility of prognosis alone highlights its moral dimensions.

	Appendix

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Members of the Steering Committee of the Research Network of the European Association of Palliative Care who also contributed to this study include the following: F. De Conno (Chair), H. Huyer Abu-Saad, A. Caraceni, N. Cherny, C.J. Furst, J. Ferraz Gonçalves, G.W. Hanks, S. Kaasa, P. Klepstad, M. Lloyd Williams, S. Mercadante, J.M. Nunez Olarte, P. Poulain, L. Radbruch, C. Ripamonti, F. Strasser, and A. Tuca i Rodriguez.

	Authors' Disclosures of Potential Conflicts of Interest

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The authors indicated no potential conflicts of interest.

	Acknowledgment

 
We thank Gráinne Tierney for editing the manuscript.

	NOTES

 
Authors' disclosures of potential conflicts of interest are found at the end of this article.

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Submitted November 23, 2004; accepted April 19, 2005.

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