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© 2002 American Society for Clinical Oncology Comprehensive Geriatric Assessment Adds Information to Eastern Cooperative Oncology Group Performance Status in Elderly Cancer Patients: An Italian Group for Geriatric Oncology StudyByFrom the Unità Operativa Geriatria Oncologica, Istituto Nazionale di Riposo e Cura per Anziani and Unità di Oncologia, Ospedale Fatebenefratelli Isola Tiberina, Roma; Divisione di Oncologia Medica and Servizio di Epidemiologia, Istituto di Ricovero e Cura a Carattere Scientifico, Centro di Riferimento Oncologico, Aviano; U.O. Oncologia Medica, Unità Sanitaria Locale 1 Imperiese, Presidio Ospedaliero, San Remo; Servizio Registro Tumori, Istituto Nazionale per la Ricerca sul Cancro, Genova; Divisione di Geriatria, Ospedale Demati, S. Angelo Lodigiano, Lodi; Divisione di Geriatria, Ospedale San Bortolo, Vicenza; Divisione di Oncologia Medica, Azienda Ospedale Università, Padova, Italy; Department of General Surgery, Whiston Hospital, Prescot, United Kingdom; and Clinique de Genolier, Genolier, Switzerland. Address reprint requests to Lazzaro Repetto, MD, U.O. Geriatric Oncology, INRCA, Via Cassia 1167, 00189 Rome, Italy; email: l.repetto{at}inrca.it
PURPOSE: To appraise the performance of Comprehensive Geriatric Assessment (CGA) in elderly cancer patients (  65 years) and to evaluate whether it could add further information with respect to the Eastern Cooperative Oncology Group performance status (PS). PATIENTS AND METHODS: We studied 363 elderly cancer patients (195 males, 168 females; median age, 72 years) with solid (n = 271) or hematologic (n = 92) tumors. In addition to PS, their physical function was assessed by means of the activity of daily living (ADL) and instrumental activities of daily living (IADL) scales. Comorbidities were categorized according to Satariano’s index. The association between PS, comorbidity, and the items of the CGA was assessed by means of logistic regression analysis.
RESULTS: These 363 elderly cancer patients had a good functional and mental status: 74% had a good PS (ie, lower than 2), 86% were ADL-independent, and 52% were IADL-independent. Forty-one percent of patients had one or more comorbid conditions. Of the patients with a good PS, 13.0% had two or more comorbidities; 9.3% and 37.7% had ADL or IADL limitations, respectively. By multivariate analysis, elderly cancer patients who were ADL-dependent or IADL-dependent had a nearly two-fold higher probability of having an elevated Satariano’s index than independent patients. A strong association emerged between PS and CGA, with a nearly five-fold increased probability of having a poor PS (ie, CONCLUSION: The CGA adds substantial information on the functional assessment of elderly cancer patients, including patients with a good PS. The role of PS as unique marker of functional status needs to be reappraised among elderly cancer patients.
THE INCREASED age-related prevalence of comorbidities and functional impairment among elderly patients may enhance the risk of treatment-related complications, as well the risk of mortality among cancer patients.1-12 The lack of sound, evidence-based information concerning the treatment of elderly patients with cancer negatively affects clinical practice.13 This prejudice has been responsible in past years for the exclusion of a relevant number of geriatric cancer patients from surgery, radiotherapy, and chemotherapy.14-15 An increasing number of individuals reach old age without measurable loss of functional capacity and free of severe medical conditions.16 These persons are as likely to benefit from standard cancer treatment as younger population groups do, but elderly patients who present with comorbid conditions and functional impairment are at a higher risk of developing treatment-related complications. They should be identified to prevent undue morbidity. On such a basis, a reliable and validated instrument capable of providing full details on comorbidities and disabilities at the time of cancer diagnosis among elderly patients is needed. The assessment of the functional status by means of the widely used Karnofsky or Eastern Cooperative Oncology Group (ECOG) scales does not seem as effective in older patients as in the adult population because comorbidities in the elderly may interfere with the measurement of the performance status (PS).17 Several instruments have been proposed to monitor comorbidities, although none has been validated or widely accepted by the oncologic community.18 Similarly, the functional status is carefully investigated in geriatrics by means of different scales that are not implemented for oncologic purposes. A Comprehensive Geriatric Assessment (CGA) scale was thus developed and validated by the Italian Group for Geriatric Oncology (GIOGer).19 This clinical research instrument was generated with the aims of avoiding arbitrary decisions on patient selection, favoring uniform treatment monitoring, and allowing better comparisons of oncologic results. The aim of this large, multi-institutional investigation of the GIOGer was to delineate the usefulness of CGA among elderly cancer patients. In this article, we report baseline data on 363 elderly cancer patients in regard to the potential association between PS, comorbidity, and the dimensions measured by CGA (ie, functional, cognitive, and emotional status).
In this cross-sectional analysis, the study group consisted of a consecutive series of 363 cancer patients (168 men and 195 women) aged 65 years or older who were admitted with a first diagnosis of cancer at one of the contributing centers (Appendix 1) between January 1994 and December 1996. The following cancer diagnoses were histologically confirmed: breast cancer (n = 112), hematologic tumors (n = 92; non-Hodgkin’s lymphomas, n = 56; acute and chronic leukemias, n = 11; Hodgkin’s disease, n = 9; myelodysplastic syndrome, n = 9; multiple myeloma, n = 7), lung cancer (n = 54); colorectal cancer (n = 47), head and neck cancers (n = 43), and others (n = 15). Solid tumors were staged according to the tumor-node-metastasis classification, and grouped in three categories (ie, local, locally advanced, and advanced). Non-Hodgkin’s lymphomas and Hodgkin’s disease were staged according to the Ann Arbor classification, although multiple myeloma were staged according to the Durie and Salmon classification. Other hematologic tumors were considered advanced diseases. One hundred forty-four subjects (39.7%) were diagnosed with localized tumors, including 22.0% patients with locally advanced disease.
The data collection was based on patient history, routine physical examination, and previous charts (when available) and was recorded on a standardized questionnaire. In each of the participating centers, trained interviewers administered the questionnaire within a median period of 3 days (range, 1 to 8 days) from patient’s admission. The questionnaire took approximately 20 minutes to be administered. Information was elicited on patient’s education (defined by a four-level scale: completed university or senior school, ie, > 8 years of education; junior school, ie, 5 to 8 years of education; primary school, ie, 5 years of education; or illiterate, ie, < 5 years of education); number of cohabitants permanently living with the patient in the month before hospital admittance (12 patients living in nursing home were considered to be living with
Statistical Analysis The statistical significance of differences among proportions was tested by means of the  2 test or, when appropriate, by means of the 2 for trend test (two-sided P  .05 as level of significance). The potential association between the PS, each item of the CGA, or the Satariano’s index was evaluated by means of ordinal logistic regression analysis. Thus, we computed multiple logistic odds ratios (OR) and their 95% confidence intervals (CI), adjusted for age and sex. The statistical significance of such OR was assessed via the likelihood ratio test.25,26
General Characteristics The median age of these 363 elderly cancer patients was 72.9 years (range, 65 to 92 years); the large majority (78.9%) of patients aged 85 years or more was constituted by women (Table 2). Overall, the degree of education was substantially low (68.9% reported < 6 years of education), and the majority of these patients tended to live alone, particularly patients aged 75 years or more (Table 2).
Comorbidity Table 3 shows the distribution of concomitant diseases according to the modified Satariano’s index, sex, and age groups. Overall, 41% of these 363 patients had one or more comorbid conditions. The frequency of comorbidities was higher in women than men (44.1% v 37.5%; P .01), although it did not increase with age (P = .28). Interestingly, none of the elderly cancer patients aged 85 years or older presented with two or more comorbid conditions. Table 1 shows the list of comorbid conditions according to prevalence.
CGA The distribution of the study population according to the dimensions measured by the CGA is summarized by age and sex in Table 4. These 363 elderly cancer patients presented with good functional and mental status as measured by the PS (74.1% of them had a PS lower than 2), the ADL scale (86.2% were independent), IADL (52.3% were independent), and MMS (normal in 72.9% of patients). Conversely, 39.9% of the patients had one or more depressive symptoms as measured by the GDS scale.
Of the 269 patients with a normal PS (ie, lower than 2), 13.0% presented with two or more comorbid conditions; 9.3% and 37.7% had ADL and IADL limitations, respectively. Approximately 30% had limitations in their mental or emotional status (Table 4). A statistically significant correlation emerged between PS, number of comorbidities, and CGA items. The correlation was particularly strong between PS and IADL (r = -.52) (Table 5).
Multivariate Analysis Elderly cancer patients who were ADL-dependent or IADL-dependent had a 1.7-fold significantly higher probability of having an increased Satariano’s index than independent patients (Table 6). Conversely, no statistically significant association emerged between the modified Satariano’s index and sex, age, PS, GDS, MMS, or tumor stage.
A stronger association emerged between PS and the four dimensions measured by the CGA variables (Table 7). A nearly five-fold increase of the possibility of having a poor PS (ie, 2) was reported for elderly cancer patients who were dependent at the ADL (OR, 5.1) or at the IADL (OR, 5.2) scale. Patients with depressive symptoms (OR, 3.7) or with cognitive impairments (OR, 2.6) were also at a significantly higher risk of having a poor PS (Table 7). These findings were not affected by patient age.
Increasing age is generally considered a major determinant of health status on its own, with a consistently reported age-related decline in functional status and an increase in disability rates.27-29 In elderly patients, functional status constitutes an important indicator of the overall health condition, reflecting the degree of an individual’s independence and his or her ability to use health care services. Moreover, functional status represents a good predictor of mortality.30-35 The clinical relevance of measuring functional status in the elderly cancer patients remains little investigated. An adequate instrument is still to be implemented, and its usefulness is still controversial. Thus, studies are urged to clarify if a more accurate evaluation can be provided by the CGA, which has proven useful in predicting mortality and disability in several clinical settings,36-40 to better tailor the treatment plan at the individual level. Clinical studies in elderly cancer patients have shown the negative impact of comorbidity on prognosis, as well as on disability,5,41-45 but few of these studies have underlined the relevance of a thorough comorbidity assessment. Thus, in elderly cancer patients, the relevance of both functional status and/or comorbidity represents a largely under-investigated area. The work herein reported represents the largest series of elderly cancer patients investigated to assess the association between comorbidity, functional disabilities, and PS by means of the CGA.46-49 There are three major findings that are worth summarizing. Firstly, a statistically significant association emerged between comorbidity as measured by the modified Satariano’s index and functional status as measured by ADL and IADL. Secondly, no association was found between PS and comorbidity. Thirdly, though PS was significantly associated with the items investigated by means of CGA, it was noticed how several aspects of functional impairment as measured by ADL and IADL were not identified by PS: between 9% and 38% of patients with good PS (< 2) had limitations detected by CGA. The frequency and types of comorbidities registered among the present group of 363 elderly cancer patients were similar to those reported by previous works in the literature for both the general elderly population and other cancer series.8-12,50 We did not observe any cancer patient aged 85 years or older affected by two or more comorbidities. It is, thus, likely that a selection bias may exist for elderly cancer subjects addressed to cancer centers. This fact had been previously registered by our group.50 The observation that comorbidity and disability measured by CGA are positively associated in the elderly with cancer and the knowledge of the prognostic role of CGA in the older patients suggest that CGA should be used with elderly cancer patients. Further studies are needed to assess whether CGA can properly address the therapeutic decision and treatment-related toxicity, thus helping to achieve a wider consensus on the instruments to be adopted. The lack of association between PS and comorbidity that emerged at multivariate analysis may be explained by the measurement of comorbidity according to the number of conditions. Although it was decided to use the Satariano’s index, because of the previously mentioned limitations of such an approach,51 no statistically significant relationship was found. A broad consensus is advocated to recommend the optimal comorbid scoring system for the older population of healthy or moderately ill subjects, as the elderly cancer patients of our series were. CGA, thus, should be performed through large follow-up cooperative studies to allow a better understanding of the indications and efficacy of chemotherapy for elderly cancer subjects. A relevant finding from our study is that PS seems to be significantly associated with functional status (ADL and IADL), as well as with the other dimensions investigated through the CGA (ie, GDS and MMS). Such a finding suggests that the clinical value of measuring ECOG-PS in elderly cancer patients might require reappraisal. We already reported how, among elderly cancer patients with good PS, 4% had ADL and 46% had IADL limitations and that a strong association exists between PS and IADL.52 These observations have clinical implications: they suggest that ADL and IADL are more sensible than the PS alone and that many aspects of functional impairment are not fully recognized by PS. In particular, the IADL scale recognizes the aspects of daily life that require instrumental activities, such as using public transportation or the telephone, that may affect adherence to diagnostic and therapeutic programs.53 On the other hand, ADL has been shown to be particularly associated with survival in previous studies.53-59 Other authors have previously attempted to identify a reliable and sensitive instrument to be used among elderly cancer patients. Extermann et al60 compared, in a univariate analysis, the Charlson comorbidity scale and the Cumulative Illness Rating Scale–Geriatric and their association with functional status measured by ECOG-PS, ADL, and IADL. Despite the large difference in sensitivity between the two scales (ie, only 36% patients who had comorbidities according to the Charlson scale v 94% with the Cumulative Illness Rating Scale–Geriatric), a consistent lack of association with functional status was reported. Extermann et al60 concluded that comorbidity needs to be assessed independently from functional status. Piccirillo and Feinstein61 recently reviewed the literature on endometrial, prostate, larynx, and rectal cancer staging, prognosis, and treatment. The impact of some comorbidities, regardless of the tumor-node-metastasis tumor stage, on 5-year survival rates was reported, and the authors concluded that concomitant diseases and symptoms provide fundamental information and should be incorporated in the clinical system of tumor classification to improve prognostic accuracy. Yancik et al11 who studied a large series of colorectal cancer patients, showed how the type and number of comorbid conditions significantly predicted 2-year mortality. Although disease stage at diagnosis was the strongest predictor of mortality, comorbidity affected both cancer management and survival duration. Satariano and Ragland1 determined the effect of selected comorbidity, including myocardial infarction and other types of heart disease, diabetes, and respiratory, gallbladder, and liver conditions and second malignancies, on the survival of breast cancer patients. A positive correlation with 3-year survival rates was reported after stratification according to the number of the selected conditions. The authors concluded that the measurement of comorbidities should be routinely considered in clinical practice. Despite such strong evidence, a standardized instrument for the measurement of comorbidities is not yet available. Moreover, different tumor types and treatment options may account for different relationships between comorbidity, disability, and prognosis. CGA has proven useful in predicting mortality and disability in several clinical settings, including hospital geriatric evaluation, inpatient geriatric consultation, home assessment service, hospital home assessment service, and outpatient assessment service and in patients with a number of chronic diseases.36-40 The findings of this GIOGer study indicate that clinical implications for cancer patients are so far not clear, and the added value to patient clinical management remains to be verified in the longitudinal analyses. Elderly patients with different forms of cancer were included in the present study to test whether the CGA approach was broadly feasible in this group of patients. No differences emerged, for instance, between patients with solid tumors and patients with hematologic malignancies. Although the patients’ heterogeneity attributable to the various types of cancer may differently affect the efficacy of the intervention, this choice allowed us to preliminarily evaluate the CGA in a wider scenario. Future studies, possibly longitudinal in design, should be tailored to assess the potential differences according to different cancer types. The CGA scale adopted in the present study is easy to apply even in unsophisticated conditions, allows collection of homogeneous information among different patients and different institutions, and has a low cost, requiring approximately 20 minutes with a trained interviewer. The lack of correlation between PS and comorbidity that emerges from this study, as recently summarized in a review paper,62 underlines the importance of the comprehensive assessment of the global health status of elderly cancer patients by means of CGA. Longitudinal studies are needed to clarify whether CGA may support therapeutic decisions tailored for each patient. In conclusion, the study findings indicate that the CGA adds substantial information to the functional assessment of elderly cancer patients routinely collected through the PS index. Among elderly cancer patients, the role of PS as unique marker of functional status needs to be revisited, and our study sheds new original light on this aspect. The impact of CGA on the life expectancy of elderly cancer patients now needs to be investigated through longitudinal evaluations.
Supported in part by the Italian Ministry of Health, Rome, and Associazione Italiana per la Ricerca sul Cancro, Milan, Italy. The following centers and physicians contributed to GIOGer: Istituto di Ricovero e Cura a Carattere Scientifico Centro di Riferimento Oncologico, Aviano: L. Fratino, D. Serraino; Istituto Nazionale di Riposo e Cura per Anziani, Firenze: I. Del Lungo, L. Ferrucci; Cattedra di Geriatria, University of Genova: C. Ivaldi; Istituto Nazionale Tumori, Genova: S. Parodi, R. Rosso, L. Santi, M. Vercelli; Policlinico, Milano: C. Vergani, G. Villa, D. Dal Lago; Azienda Ospedale Università, Padova: S. Monfardini; INRCA, Roma: L. Repetto; University La Sapienza, Roma: W. Gianni, V. Marigliano; Ospedale Fatebenefratelli Isola Tiberina, Roma: V. Zagonel; USL 1 Imperiese, PO Sanremo: A.Venturino; Ospedale S. Bortolo, Vicenza: F. Gioia; Whiston Hospital, Prescot, United Kingdom: R.A. Audisio. We thank Jan Woodhouse and Ann Rimmer, Education and Training Department, Whiston Hospital, Prescot, United Kingdom, for their careful assistance in editing the final draft of the manuscript.
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Copyright © 2002 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
