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Journal of Clinical Oncology, Vol 25, No 22 (August 1), 2007: pp. 3313-3320 © 2007 American Society of Clinical Oncology. DOI: 10.1200/JCO.2006.10.5411 Survival Prediction in Terminally Ill Cancer Patients by Clinical Estimates, Laboratory Tests, and Self-Rated Anxiety and Depression
From the Department of Radiation Oncology; Clinic and Institute for Psychosomatic Medicine and Psychotherapy; and the Institute of Biostatistics, University Hospital Düsseldorf at Heinrich-Heine-University, Düsseldorf, Germany Address reprint requests to Stephan Gripp, MD, Department of Radiation Oncology, University Hospital Düsseldorf at Heinrich-Heine-University, Düsseldorf, Moorenstrasse 5, D-40225 Düsseldorf, Germany; e-mail: stephan.gripp{at}uni-duesseldorf.de
Purpose To study how survival of palliative cancer patients relates to subjective prediction of survival, objective prognostic factors (PFs), and individual psychological coping. Patients and Methods Survival was estimated according to three categories (< 1 month, 1 to 6 months, and > 6 months) by two physicians (A and B) and the institutional tumor board (C) for 216 patients recently referred for palliative radiotherapy. After 6 months, the accuracy of these estimates was assessed. The prognostic relevance of clinical symptoms, performance status, laboratory tests, and self-reported emotional distress (Hospital Anxiety and Depression Scale) was investigated.
Results In 61%, 55%, and 63% of the patients, prognoses were correctly estimated by A, B, and C, respectively. Conclusion This study revealed that physicians' survival estimates were unreliable, especially in the case of patients near death. Self-reported emotional distress and objective PFs may improve the accuracy of survival estimates.
Clinical prediction of survival (CPS) in cancer patients is among the most challenging tasks that physicians face. It refers to a procedure in which the judge puts clinical data together using informal, subjective methods. The nature of this process tends to preclude precise specification.1 CPS inherently has a decisive impact on a variety of treatment decisions. Correct survival estimates in terminally ill patients help to prevent inappropriate therapies and to avoid unnecessary toxicity. For instance, radiotherapy fractionation is tailored to the need for rapid onset of palliation and, on the other hand, to the probability of late adverse reactions. In addition, rendering an accurate prognosis is an integral part of the support for patients and their families and is required for timely referral to hospice care. From a public point of view, the ability to determine correct prognosis is important for the conduct of research programs and for prioritization of health care resources. Prognostic factors (PFs; ie, objective indicators of survival) are essential for implementation of CPS to evidence-based clinical practice guidelines.2 Traditional PFs (eg, stage, histology, or receptor status) can reasonably predict survival in early-stage disease but do not provide an adequate short-term prognosis in patients with advanced cancer.3 Near the end of life, nonspecific life-threatening complications may intervene regardless of the underlying disease (eg, malnutrition, cachexia, thromboembolism, or bleeding). Usually, prognosis is derived from CPS, patient signs and symptoms, and laboratory tests.4 In this study, CPS, PFs, and the impact of psychological disorders on survival were examined in cancer patients treated at a single academic radiation oncology institution.
The Radiation Oncology Department at the University Hospital Düsseldorf is the largest of three radiation therapy units in the Düsseldorf district, with approximately 600,000 inhabitants. We provide the entire spectrum of palliative and curative radiation treatments. Approximately 1,300 in- and outpatients are seen at our institution per year. Referrals come from affiliated hospitals and general practitioners embracing all specialties. The accrual period of this study was set to 6 months for an expected 200 eligible patients. From December 2003 to July 2004, 786 patients were seen at our institution. Adjuvant or curative treatments, comprising approximately 60% of referrals, were excluded. From the remainder, 228 patients were approached, and 216 consented to participate in this prospective cohort study. The protocol was approved by an institutional ethics committee. Three independent survival estimates were obtained at the beginning. One assessment was given by the doctor caring for the patient. The majority of these were doctors in training (n = 11, 83% of the ballots), whereas only a few were qualified radiation oncologists (n = 4, 17% of the ballots). The median professional experience of these 15 pooled physicians was 1.7 years (range, 0.4 to 18.3 years) from inception of training in radiation oncology. The second prognosis was obtained from a single experienced physician (S.G.) who worked more than 10 years in radiation oncology. After a brief informal discussion of the patient among all physicians attending the institutional panel, the third prognosis was obtained by a consensus vote. In this conference, which was chaired by the head of the department, depending on the daily work load, approximately five to 10 staff physicians met. The appraisals of survival time were assigned to one of the following three categories: less than 1 month, 1 to 6 months, or more than 6 months. Admittedly, these intervals are to some extent arbitrary, but they meet special needs in palliative radiation therapy, such as hypofractionation for rapid symptom relief (prognosis < 1 month.) and consideration of late radiation damage (prognosis > 6 months). To prevent biased appraisals, the ballots were kept confidential and were neither discussed with nor communicated to patients. In a brief interview and check of the medical records at study entry, one author (S.M.) recorded diagnosis, number and site of metastases, performance status (Karnofsky performance status [KPS]5 and Eastern Cooperative Oncology Group [ECOG] scale6), pain and use of analgesics, dyspnea, weight loss, nausea, and fatigue. In addition, psychological distress was studied using the Hospital Anxiety and Depression Scale (HADS), a validated psychometric self-assessment test comprising 14 questions related to anxiety and depression.7,8 The HADS is a clinical screening tool for identifying and quantifying the most common forms of psychological disturbances. In this test, physical symptoms, such as headache and weight loss, that may be confused with somatic symptoms of the current disease (eg, brain metastases) are omitted. Patients who were not fit enough to cope with or who refused the questionnaire were jointly scored as "no answer." The relevance of blood glucose, the serum enzymes of alkaline phosphatase and lactate dehydrogenase (LDH), the function parameters of creatinine, bilirubin, and C-reactive protein, and blood count including hemoglobin were also studied.
Six months after study entry, the health status was checked by personal telephone call to the patient or the relatives or by inquiry to the local residents' registration office. Statistical analyses were performed using SAS version 9.1 (SAS Institute, Cary, NC). The agreement of predictions with actual survival was analyzed using the McNemar test and was measured with Life-table analysis with log-rank test was applied in univariate analyses to clinical and laboratory parameters. Cutoff values were adopted according to common recommendations and the reference ranges of the laboratory. The Bonferroni correction was applied for multiple comparison procedures. Finally, variables significant at a 5% level in univariate analysis adjusted to multiple comparisons were entered into standard multiple regression equations to identify the salient factors predicting survival. Stepwise Cox regression analysis was performed, and hazard ratios (HRs) were calculated.
The median age of the 216 participating patients was 64 years (range, 21 to 96 years), and 51% (n = 110) were male. The most frequent principal diagnoses were lung cancer (25%, n = 55), breast cancer (24%, n = 52), head and neck cancer (9%, n = 19), lymphoma (7%, n = 15), and colorectal cancer (5%, n = 10). The median ECOG performance status score was 2, corresponding to less than 50% of the time bedridden. The median survival time was 169 days. Thirty-three patients (15%) died within 1 month, 78 (36%) died between 1 and 6 months, and 105 (49%) lived beyond 6 months. Most patients (90%, n = 194) presented with metastatic/systemic disease; the remainder suffered from incurable locally advanced cancer. Complete blood tests were available in 198 patients (92%). Missing blood counts were a result of incomplete or unavailable blood tests by the referring physicians or denial of puncture by the patient. Survival estimate could not be obtained in two patients because of rapid death. HADS questionnaires were completed by 154 patients (71%).
Survival Estimates
Univariate Analysis On univariate analysis (Table 2), 11 of 27 variables were significant at a 5% level adjusted for multiple testing. A poor general health status assessed by either KPS or by the ECOG score was associated with a significantly reduced survival probability. Colorectal and breast cancer conveyed a superior prognosis (Fig 3) compared with lung cancer. Among self-reported symptoms, fatigue, dyspnea at rest, and use of strong analgesics as well as depression and anxiety, as assessed by the HADS questionnaire, were associated with a significantly impaired survival. Brain metastases nearly halved the survival probability at 180 days. Leukocytosis and elevated LDH connoted a decreased survival. Abnormal platelet count, hyperglycemia, and reduced appetite were borderline significant prognosticators. The residual variables tested, including clinical symptoms (nausea, weight loss, body mass index, and pain), metastatic spread to specific organs (bone metastases, lung metastases, and liver metastases), and hematologic parameters (platelet count, blood glucose, C-reactive protein, anemia, creatinine, alkaline phosphatase, and bilirubin), did not significantly affect survival.
Multivariate Analysis Those parameters significant on univariate analysis at a 5% level were put in a stepwise Cox regression analysis. Primary colorectal cancer (HR = 0.16; 95% CI, 0.04 to 0.64; P = .01) and breast cancer (HR = 0.43; 95% CI, 0.25 to 0.74; P = .002) had a relatively favorable prognosis compared with other primary tumors. Metastatic spread to the brain (HR = 1.78; 95% CI, 1.14 to 2.78; P = .011), KPS less than 50% (HR = 2.49; 95% CI, 1.62 to 3.83; P < .0001), use of morphine (HR = 1.65; 95% CI, 1.08 to 2.52; P = .02), dyspnea (HR = 1.67; 95% CI, 1.06 to 2.64; P = .029), abnormal LDH (HR = 2.40; 95% CI, 1.59 to 3.63; P < .0001), and elevated WBC (HR = 1.68; 95% CI, 1.09 to 2.58; P = .019) conveyed a significantly inferior prognosis (Fig 4).
CPS is among the most problematic ongoing challenges that doctors deal with in clinical practice.10 However, many treatment decisions rely on survival estimates. Fractionation schedules in radiotherapy are strongly influenced by expected survival and the probability of long-term complications such as radiation myelitis. Missing the terminal phase of the disease may also give rise to hospital admissions at the cost of dying at home.11 Although a few objective instruments for prediction of survival in hospitalized patients with late-stage cancer12,13 and outpatients14 have been developed, CPS is predominantly founded on informal personal guesses.15 However, most physicians' prognoses tend to be both imprecise and overly optimistic.16-18 In a large prospective cohort study comprising 343 doctors and 468 terminally ill patients with a median survival time of 24 days, 63% of prognoses were overoptimistic (ie, the prognosis exceeded more than 1.5x the actual survival).19 Even experienced oncologists acknowledge their uncertainty.20
In the present study, the survival periods (< 1 month, 1 to 6 months, and > 6 months) of 216 patients referred to palliative radiotherapy for advanced cancer were independently estimated by three professionals, one intern of the medical staff, an experienced radiotherapist, and the institutional tumor board. Categories, rather than traditional continuous estimates, may improve prediction accuracy,21 and similar categoric criteria are customary to provide access to hospices and palliative care units.22 All of the staff members were professionals working in radiation oncology for some time. CPS was correctly assessed in 55% to 63% of patients. Although the number of raters is too small to draw statistically meaningful conclusions, the experienced physician with more than 10 years of professional experience was obviously no more accurate, but the estimation errors were symmetrically distributed. In contrast, the CPS of the interns and the institutional tumor board was overly optimistic. One potential criticism of the study is that the treating physicians had little time to get to know the patients and the panel estimate was based on the records only. However, extended clinical experience, medical education, and a strong doctor-patient relationship do not seem to improve accuracy of CPS.3,19,23 On the contrary, disinterested doctors with less patient contact may give even more accurate prognoses.24 In particular, optimistic expectations cloud the reality of imminent death. Survival of patients who died within 1 month was correctly predicted in only 4.4% to 29% of patients. In fact, 17% to 23% of these patients were expected to live for more than 6 months. Comparable findings were obtained with five outpatient hospice programs comprising 343 doctors and 468 terminally ill patients despite a considerably lower median survival time of 24 days compared with our study. CPSs were correct in 20% of patients, 63% of CPSs were overoptimistic, and 17% of CPSs were too pessimistic.19 The prognostic error was inversely correlated with actual survival. These findings were corroborated in a Canadian study22 on 233 patients seen at the onset of their terminal phase. Almost half of the patients were not assigned to the correct survival category (< 2 months, 2 to 6 months, and > 6 months), similar to our study. Weighted Most of the objective PFs in early-stage cancer are site and disease specific (eg, axillary node status in breast cancer or prostate-specific antigen in prostate cancer). In the terminal phase of cancer, specific parameters become less important than in early disease.25 In many studies, it has become clear that general overall condition is a major predictor of the outcome, either measured as ECOG status or KPS.12,13,25-28 Primary tumor, brain metastases, fatigue, leukocytosis, elevated LDH, and shortness of breath have proven to impact on survival in our study as well as in other studies.14,29 We found that a KPS of less than 50% predicts a median survival time of 95 days in our study compared with a median survival time of less than 8 weeks found by others.4 Recently, CPS, KPS, anorexia, dyspnea, WBC count, and lymphocyte percentage have been combined into a palliative prognostic score30 to predict survival at 30 days. This score has been validated on an independent patient series.12 In addition, we found the use of strong analgesics, but not pain alone, to be associated with impaired survival. Emotional disorders have been detected in a large proportion of cancer patients. In a random sample, up to 47% of patients received a formal diagnosis according to the American Psychiatric Association's Diagnostic and Statistical Manual of Mental Disorders, 3rd Edition diagnostic system.31 Approximately 85% of these patients were experiencing a disorder with depression or anxiety. However, the prevalence varies widely by study and is often attributable to differences in assessment procedures, diagnostic methods and approaches, patient selection, stage and type of cancer, and timing of assessment. In general, screening tests in cancer patients report an incidence of psychological disorders in a wide range of between 10% and 50%.31-36 The HADS,7 which is based on a standardized questionnaire for self-examination, is an easily administered validated screening tool developed to identify cancer patients in nonpsychiatric hospital departments as having high levels of anxiety or depression.32 It has a proven good predictive value for affective disorders in patients with advanced breast cancer37 and has also been validated in a variety of other malignant and nonmalignant diseases.38,39 The influence of coping and emotional distress on survival in cancer patients is controversial. In a prospective study on 103 lung cancer patients, depressive coping before commencement of treatment was associated with a significantly shorter survival.40 Depressed mood assessed by HADS in medical inpatients also predicted mortality.41 Several mechanisms have been proposed to explain how depression may potentially impair the course of disease, including dysregulation of the hypothalamic-pituitary-adrenal axis42 and effects on immune response that may affect cancer surveillance.43 In addition, low compliance as a consequence of emotional disorders may reduce treatment success.44 Thus, there is evidence of a bidirectional relationship between cancer and depression. We found a strong impact of psychological distress, namely depression and anxiety, on survival. However, on multivariate analysis, no independent significance emerged. General conclusions must be interpreted with caution because the low response rate of approximately 70% indicates patient selection that may distort the results of multivariate analysis. Physicians are reluctant to frankly communicate their survival assessments to the patient and family. In a study on 326 terminally ill patients, physicians overstated the prognoses communicated to the patients by a factor of 1.2 compared with the confidentially formulated prognoses. Physicians favored providing an apparently knowingly inaccurate prognosis for 40.3% of patients.45 To avoid this disclosure bias, we decided to use confidential prognoses only. Disclosing prognosis to patients and relatives is a matter of controversial debate.46 It is argued that patients want accurate estimates of their prognosis, allowing them to make end-of-life plans. However, thoughtfully delaying or avoiding prognostic information may preserve the patient's hope. In our opinion, a rarely discussed47 but critical point is the considerable inaccuracy of medical prognosis. Even if objective scores may improve prognostic certainty, the doctor's personal judgment will most likely be communicated when counseling the patient. In our study, a small minority of patients who died within a month would have been correctly informed by the treating physicians. In the absence of empirical data on the impact of false-positive or -negative prognoses on emotional distress and quality of life, vague prognostic information allowing for major individual deviations and explicitly emphasizing the uncertainty of medical prognoses seem to us to be most appropriate when counseling patients.
The author(s) indicated no potential conflicts of interest.
Conception and design: Stephan Gripp, Sibylle Moeller, Matthias Franz, Reinhardt Willers Administrative support: Stephan Gripp, Sibylle Moeller, Gerd Schmitt, Wilfried Budach, Reinhardt Willers Provision of study materials or patients: Stephan Gripp, Sibylle Moeller, Gerd Schmitt, Christiane Matuschek, Sonja Asgari, Farzin Asgharzadeh, Stephan Roth, Edwin Bölke, Matthias Franz Collection and assembly of data: Stephan Gripp, Sibylle Moeller, Reinhardt Willers Data analysis and interpretation: Stephan Gripp, Sibylle Moeller, Edwin Bölke, Gerd Schmitt, Christiane Matuschek, Wilfried Budach, Matthias Franz, Reinhardt Willers Manuscript writing: Stephan Gripp, Sibylle Moeller, Edwin Bölke, Reinhardt Willers Final approval of manuscript: Stephan Gripp, Edwin Bölke, Wilfried Budach, Matthias Franz, Reinhardt Willers
We thank James Kilbury, Düsseldorf, Germany, and Daniel Roos, MD, Royal Adelaide Hospital, Adelaide, Australia, for patient discussions and invaluable support preparing the article. We also acknowledge U. Kretschmar; S. Doll, MD; H. Pape, MD; H. Ribbert, MD; S. Röger; M. Wittkamp, MD; A. Landegehm, MD; and M. Daum, MD, for their estimates of patient survivals.
Presented in part at the 42nd Annual Meeting of the American Society of Clinical Oncology, June 2-6, 2006, Atlanta, GA. Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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Zubrod C, Sheiderman M, Frei E: Appraisal of methods for the study of chemotherapy in man: Comparative therapeutic trial of nitrogen mustard and triethylene thiophosphoramide. J Chronic Dis 11:7-33, 1960 7. Zigmond AS, Snaith RP: The hospital anxiety and depression scale. Acta Psychiatr Scand 67:361-370, 1983[Medline] 8. Herrmann C, Buss U, Snaith P: HADS-D: Hospital Anxiety and Depression Scale–Deutsche Version. Ein Fragebogen zur Erfassung von Angst und Depressivität in der Somatischen Medizin. Bern, Switzerland, Hans Huber, 1995 9. Landis JR, Koch GG: An application of hierarchical kappa-type statistics in the assessment of majority agreement among multiple observers. Biometrics 33:363-374, 1977[CrossRef][Medline] 10. Christakis NA, Iwashyna TJ: Attitude and self-reported practice regarding prognostication in a national sample of internists. Arch Intern Med 158:2389-2395, 1998 11. 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Hopwood P, Howell A, Maguire P: Screening for psychiatric morbidity in patients with advanced breast cancer: Validation of two self-report questionnaires. Br J Cancer 64:353-356, 1991[Medline] 38. Ibbotson T, Maguire P, Selby P, et al: Screening for anxiety and depression in cancer patients: The effects of disease and treatment. Eur J Cancer 30A:37-40, 1994[CrossRef] 39. Herrmann C: International experiences with the Hospital Anxiety and Depression Scale: A review of validation data and clinical results. J Psychosom Res 42:17-41, 1997[CrossRef][Medline] 40. Faller H, Bulzebruck H: Coping and survival in lung cancer: A 10-year follow-up. Am J Psychiatry 159:2105-2107, 2002 41. Herrmann-Lingen C, Klemme H, Meyer T: Depressed mood, physician-rated prognosis, and comorbidity as independent predictors of 1-year mortality in consecutive medical inpatients. J Psychosom Res 50:295-301, 2001[CrossRef][Medline] 42. 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J Clin Oncol 23:3146-3150, 2005 Submitted December 27, 2006; accepted May 10, 2007.
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Copyright © 2007 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
statistic showed fair agreement of the estimates, which proved to be overly optimistic. Accuracy of the three estimates did not improve with increasing professional experience. In particular, the survival of 96%, 71%, and 87% of patients who died in less than 1 month was overestimated by A, B, and C, respectively. On univariate analysis, 11 of 27 parameters significantly affected survival, namely performance status, primary cancer, fatigue, dyspnea, use of strong analgesics, brain metastases, leukocytosis, lactate dehydrogenase (LDH), depression, and anxiety. On multivariate analysis, colorectal and breast cancer had a favorable prognosis, whereas brain metastases, Karnofsky performance status less than 50%, strong analgesics, dyspnea, LDH, and leukocytosis were associated with a poor prognosis. 
