| | Prescribers’ attitudes toward elderly breast cancer patients. Discrimination or empathy?Accepted 24 September 2009. published online 26 October 2009. Abstract Advancing age is often associated with co-morbidities. Patients’ chronological and physiological ages do not always correspond. Elderly patients are often excluded from clinical trials and given sub-optimum treatment. In this context, the question of equity in access to health care arises. A specially designed questionnaire was mailed to French oncologists to determine what factors influenced them and to elicit their medical practice using four clinical cases. Significant differences in treatment choice depending only on patient's age were observed. The likelihood of an elderly breast cancer patient undergoing chemotherapy was found to depend on physician specialty and gender, kind of care structure, physician's perception of the age at which patients become elderly, and their knowledge about geriatric assessments. Some physicians did not always prescribe potentially beneficial treatments when dealing with elderly patients. Given the multidimensional nature of the care process, patients’ preferences should be taken into account in medical decision-making. 1. Introduction  Questions about the most appropriate medical strategies for dealing with elderly breast cancer (BC) patients have given rise to considerable debate. Studies mainly based on the observation of medical charts have shown the existence of significant differences in access to treatment, depending on the patients’ chronological age [1], [2], [3], [4], [5]. Older patients are often not given adjuvant treatments such as chemotherapy and radiotherapy [1], [6]. The main question which arises is whether an arbitrary age limit [7] should continue to be adopted as a basis for giving patients access to some therapeutic procedures [2], [8], [9], [10]. The exact reasons for the disparities in treatment decisions have not been elucidated. Some authors have suggested that age-related differences are due to some form of ageism; while others have claimed that more rational criteria are involved [11]. For example, the fear that the toxicity may be greater in older patients may discourage clinicians [12] from prescribing chemotherapy, especially as hormonotherapy seems to be particularly efficient on this population [13], [14], [15]. However, given the success of adjuvant chemotherapy on menopausal women, there are no biological reasons for not extending the benefits of this treatment to older patients if the vital prognosis is not restricted by other diseases and if the treatment seems likely to be well tolerated [16], [17], [18]. Moreover, if studies have not found any impact of undertreatment in term of rates of recurrence and mortality [1], [19], [20], others have suggested a negative impact of less than standard treatment [16], [21]. As recently stated by Enger et al. [22], several factors have been investigated with a view to explaining these differences in patients’ management, such as patients’ demographic and clinical characteristics, the patient–physician relationship, and patients’ and caregivers’ preferences, including integrating health care setting. To our knowledge, if some studies have studied surgeons’ characteristics [23], [24], [25], the characteristics of the oncologists themselves have not yet been explored. To determine whether or not discriminatory practices exist (based on the question of horizontal equity: same treatment for similar patients), a sample of French medical oncologists and radiotherapists were questioned about their decision-making criteria when dealing with non-metastatic BC patients aged 70 years or more. The aim was to identify any relevant physicians’ characteristics, such as their socio-demographic characteristics, experience, awareness of geriatric tests, “practice-style effects [26]” and belief in the efficacy of the various adjuvant treatments available, which might affect the medical decision-making process when dealing with this specific population. 2. Materials and methods A specially designed questionnaire was sent out to 14081 French medical oncologists and radiotherapists in the private and public sectors potentially treating BC patients, and then in particular women over 70 years of age. This anonymous questionnaire was mailed along with an explanatory letter and a pre-stamped and labeled envelop. Two reminders were made if necessary: first by phone, one month after the questionnaire was sent; and then by mail along with another copy of the questionnaire, two months later. The topic under investigation seemed to be important enough to justify not giving any financial compensation for completed questionnaires. To be included in the survey, physicians had to have treated at least five women aged 70 years or more with non-metastatic BC during the previous year. 2.1. Questionnaire A two-part questionnaire was used to test our hypothesis of a potential barrier preventing older BC patients from having access to adjuvant treatment might be partly due to physicians. The first part focused on the physicians’ characteristics and the second part, on the elicitation of their medical practice toward four specific clinical cases. The use of written cases to measure propensity to prescribe a particular adjuvant treatment has the advantage of controlling for disease and patients attributes [25], [31]. 2.1.1. Characterization of physicians and their perception of elderly BC patients The physicians’ socio-demographic and professional characteristics were used to characterize the sample and to determine whether factors such as professional experience, number of patients treated, reading scientific articles, and participating in medical vocational training courses might have affected their medical decision-making processes. Since the perception of who constitutes an elderly patient depends on each physician, they were asked to state the age above which they had the impression of dealing with elderly women. In addition, we asked them to specify the surgical act and the sequence of adjuvant treatments they prescribed most frequently to deal with this specific population (to determine whether they tended to prescribe any specific adjuvant treatment). Questions were also asked about how their decisions were usually taken (at pluri-disciplinary meetings, after consulting a geriatrician for advice, etc.) as well as about decision-making criteria they felt to be decisive. Lastly, since the literature suggests the need for comprehensive geriatric assessments [27], [28], [29], [30] before initiating any treatment, physicians’ knowledge about seven geriatric tests was rated by asking the respondents to state whether they knew about each test and whether they used it (Table 2). 2.1.2. Medical management of four specific clinical cases The physicians’ medical practices were elicited by presenting them with four clinical cases (Appendix A). The main patient-related variables were age, hormonal status, lymph nodes involved, size of tumor, presence of associated disease and familial context. The clinical cases presented were all cases where chemotherapy (CT) could possibly be prescribed. The expected benefits (proportional risk reduction rate) of CT administration in terms of global and disease free survival were rated using the “adjuvant online” decision tool: https://www.adjuvantonline.com/index.jsp (version 8.0) (Appendix B). Each of these cases was designed to test one specific point. 2.1.2.1. Case A to test the existence of purely age-related effects This case was randomly distributed among the respondents: in half of the questionnaires, the patient's age was changed (55 vs. 76 years old) in order to determine whether there existed a specific age-related effect: the hypothesis tested here was that patients’ age, irrespective of their medical status, may affect the treatments prescribed. 2.1.2.2. Case B to test the trade-off between hormonotherapy and chemotherapy Since it has been often stated in the literature that the decision not to prescribe CT to elderly BC patients is mainly based on the fact that hormonotherapy (HT) is particularly efficient among this population, we presented the physicians with a case where CT was highly suitable because of the patient's negative hormone receptor status. The point tested here was whether or not CT was prescribed when HT was not indicated. 2.1.2.3. Case C to test the age above which patients were perceived as being elderly CT is strongly/definitely recommended for SBR grade III patients with a 30-mm sized tumor. The patient's age in this case was at the threshold of old age (71 years old), which made it possible to test physicians’ perception of who is elderly and what impact this perception may have. 2.1.2.4. Case D to test the trade-off between chronological age and menopausal status In this case, CT may not be advisable, although the patient was described as being only 55 years old (age chosen because of the corresponding menopausal status). The question tested here was the importance of menopausal status versus age. In addition, the physicians were asked to specify how they would make their decisions in each case (alone or after consulting other specialists, or at a multidisciplinary meeting) and what their main decision-making criteria would be (age, tumor characteristics, antecedents or lack of alternatives). 2.2. Statistical analysis Based on the results obtained on all the items in the first part of the questionnaire, the physicians’ characteristics and their attitudes toward elderly BC patients were systematically compared in terms of sex, age, specialty and the kind of structure where they practiced. Only significant differences are presented. Discrete data were compared using Pearson's χ2 tests and continuous data, using Student's t-test or the Mann–Whitney U-test (SPSS 12.0 package). Since proportion of radiotherapy (RT) and hormonotherapy (HT) intention of prescription were similar among cases (Table 3), multivariate analysis was performed only on reported CT prescriptions (the dependent variable) for each of the cases. To determine the factors explaining the prescription of CT, we included all potential factors and their interactions in four logistic regression models (significance level p <0.05). The odds ratio gives the odds of prescribing CT. 3. Results Among the 565 eligible physicians (which have treated at least five BC women aged 70 years or more during the previous year) contacted, 388 (69%) completed and returned their questionnaires (see Fig. 1). 3.1. Physicians’ characteristics and attitudes toward elderly BC patients Physicians’ characteristics, perceptions and attitudes toward elderly BC patients are presented in Table 1. The main decision-making criteria they used and their knowledge about geriatric tests are presented in Table 2. 3.1.2. Perceptions and attitudes toward elderly BC patients The respondents did not agree about the age at which patients are perceived as being elderly (range: 60–90 years, average 73.3 years). The cut-off was at an earlier age among physicians from CCCs (72.2 vs. 73.7, p<0.005); whereas the great majority of the physicians (85.6%) agreed that there is a need for therapeutic trials specifically designed for elderly populations. The sequence of treatment most frequently prescribed (70.9%) when dealing with this population was ‘surgery, radiotherapy and hormonotherapy’. Conservative surgery was the main surgical act performed on tumors (68%). Frequencies of axillary dissection (44.8%) and sentinel node removal (35.8%) were fairly similar. 3.1.3. General decision-making criteria used with elderly BC patients 41% of the physicians stated that they always used the same clinical decision-making criteria (such as number of lymph nodes, hormonal status, size of tumor) as with younger patients, 46.1% of the sample felt that the decision criteria used depended on each patient, and only 10.3% said that they used specific criteria. Whatever the decision criteria adopted, 90.2% of the sample ‘often’ or ‘always’ took decisions about the treatment with a pluri-disciplinary committee, but only 17% ‘often’ or ‘always’ in contact with a geriatrician. Medical oncologists (20% vs. 11.7%) and physicians working at academic establishments or CCCs (23% and 21% vs. 8%) contacted geriatricians significantly more frequently than the others (p<0.05). Among the decision criteria thought to be important, a higher proportion of men were concerned by the patient's opinion (83% vs. 75.2%, p<0.1). A higher proportion of medical oncologists indicated that ‘dependence for social activities’ and ‘social context’ were important criteria (50.8% vs. 30.9% and 45.2% vs. 34.6%, respectively, p<0.05). These criteria were felt to be less important by physicians working at private structures (33.3% vs. 44.5% and 33.3% vs. 43%, p<0.05). ‘Social context’ was significantly more often quoted by physicians from CCCs (51% vs. 36.1%, p<0.001). Medical oncologists most frequently took ‘the opinion of a geriatrician’ and ‘poly-medication’ (25.4% vs. 17.8% and 32% vs. 24.1%, p<0.1) into account; whereas physicians from private structures were those who tended least frequently to ask for the ‘opinion of a geriatrician’ (8.9% vs. 27.5%, p<0.001). 3.1.4. Knowledge about geriatric assessments and their use Geriatric tests are presented in decreasing order of physicians’ knowledge and the use they made of each one (Table 2). Five of these tests were known by 60–67% of the sample and one by half of the sample. The test the less know (and also used) was IADL. Generally we can observe a quite low rate of use of these tests although our sample included only physicians treating elderly BC patients. The rates of knowledge and use of some geriatric tests were higher among physicians who read more scientific journals each month: this difference was significant in the case of ADL, IADL, MNA and TMS. A higher proportion of medical oncologists used each of the geriatric tests, but this difference was significant only for MMT and TMS. 3.2. Clinical cases The respondents’ answers about the four clinical cases are summarized in Table 3. The differences between the proportions of those opting for CT for each of the clinical cases were all statistically significant except between A2 (a 76-year-old patient) and B (a 78-year-old patient). Case A (55-year old patient vs. 76-year old patient): Confirmation of the age effectA significant difference was observed in the proportions of CT prescription, depending on the patients’ age (99% vs. 60.4%, p<0.001). Despite this salient difference, 71% of the physicians to whom the case of the 76-year-old patient (A2) was presented declared that they based their decision on the tumor characteristics, whereas only 14% based it on age. Case B: Efficacy of HT alone does not explain by itself CT administration barrierOne rather surprising result obtained was that 29 (7.5%) of the physicians said they would prescribe HT for this negative hormonal receptor patient. The other surprising result was the low proportion of physicians (55.5%) who opted for CT although HT is not appropriate in this case. However, this low proportion was due to radiotherapists and not to medical oncologists (43.2% vs. 66.9%, p<0.000). One should observe that if radiotherapists rather based their decision on the age of this patient (34%), medical oncologists were more concerned by tumor characteristics (45.8%). Case C: Being at the threshold age might be a barrier to CT administrationA significantly lower proportion of the physicians opted for CT for this patient than for patient A1. However, this proportion was significantly higher than with patient A2, which shows how difficult it is to make decisions at this threshold age, and how variable physicians’ perceptions can be about who is elderly and who is not. Once again medical oncologists declared they would prescribe CT significantly more often than radiotherapists (80.8% vs. 70.3%, p=0.023). Case D: Age had a greater impact than menopausal statusDespite this patient's menopausal status, she obtained the highest response rate in favor of CT apart from the other 55-year-old patient (A1). 3.3. Explicative factors of chemotherapy option in each case The likelihood of declaring to prescribe CT to the 76-year-old patient (A2) increased when the prescriber was a woman, had a propensity to administer CT to elderly patients, knew and used IADL, and with the age at which physicians regarded patients as being elderly (Table 4). The physicians in favor of CT for the 78-year-old patient (B) tended to be medical oncologists having a propensity to prescribe CT for elderly patients and taking impact of treatment on quality of life into account. It is also worth noting that having been given the oldest patient (A2) as their first case decreased the probability of prescribing CT for this patient. In the case of patient C, once again being a medical oncologist and having a propensity to administer CT increased the probability of prescribing CT, as did using the same decision-making criteria as with younger patients, and having some geriatric knowledge such as taking nutritional status into account and number of geriatric assessments known. Surprisingly, being an oncologist at a CCC decreased the probability of prescribing CT as well as taking the family's opinion into account. Case D was presented mainly as informative purpose, since this model is not very predictive. It is worth noting, however, that in this case, contrary to what was observed with two of the other cases, being a medical oncologist and taking the impact of treatment on the patients’ quality of life into account reduced the probability of prescribing CT. The positive impact of taking co-morbidities to be an important DC is also worth noting. 4. Discussion In this survey, which was conducted on a large sample of medical oncologists and radiotherapists treating elderly BC patients, some of the physicians’ characteristics (such as gender, specialty and health structure) were found to be independently correlated with the probability of opting for CT. This finding, in accordance with results from surveys interested by the relation between surgeons’ characteristics and medical practice [23], [24], [25], raises questions about providing elderly cancer patients with optimum medical care. It should be noted that actual practice can also be influenced by others factors such as patient-physician relationship [32] that could not be reflected when written clinical cases are used, as well as social desirability or non-response biases. Whatever our results on intention of treatment are consistent with results of surveys based on medical charts which have shown that older patients are undertreated, such as results from Du et al. about chemotherapy administration [33]. Despite these limits, our results allow us to give some complementary arguments to such surveys. The respondents’ answers about the four clinical cases clearly show that they tended to (declare to) prescribe chemotherapy less frequently as the patients’ chronological age increased (even when hormonotherapy was not indicated), while previous data [34] and “adjuvant online” have indicated therapeutic equivalence between older and younger BC patients (for these 4 specific cases). That is to say, we are dealing with a problem of horizontal rather than vertical equity. Our results suggest several possible explanations such as a problem of representation (of elderly patients themselves as well as expected benefits of combined adjuvant treatments among elderly patients) and some practice style effects. In addition, it seems likely that a sort of halo effect or anchoring effect [35], [36] may have been captured. Of course, our results had to be generalized among non-French oncologists. The first point to emerge from the univariate and multivariate analyses was the great variability of the age above which physicians regarded patients as being elderly. It confirms that chronological age should no longer be a decision-making criterion, as previously pointed out in the context of colorectal cancer (treatment disparities were found to be based on chronological age rather than on co-morbidities) [37]. How patients’ physiological age is defined therefore requires further attention. In the increasing body of literature on the optimum care of elderly cancer patients, the accent has been placed on potential advantages of the use of specific geriatric assessments [27], [28], [29]. Despite this awareness, our results show that few physicians are in contact with a geriatrician or familiar with geriatric tests (including the most specific one, IADL: instrumental activity of daily living), although these tests can be used to identify elderly patients liable to benefit from combined chemotherapy and hormonotherapy in addition to surgery and radiotherapy. Multivariate analysis showed how physicians’ knowledge about these geriatric assessments affected their (theoretical) decision to prescribe CT or not: knowing and using IADL, number of geriatric tests knew and regarding nutritional status as an important DC increased the probability of opting for CT. Another explanation for the physicians’ intention to prescribe CT, or not, is the existence of a pattern (propensity) of CT prescription: being an oncologist and regularly prescribing CT (in general practice toward elderly BC patients) as part of the usual sequence of treatment increased the probability of prescribing CT for the three oldest patients. Using the same clinical DC as on younger patients also increased this probability. The literature also provides rational reasons based on the efficacy of hormonotherapy on this specific population. However, based on the results from “adjuvant on line”, it is only by combining CT with HT that the same proportional risk reduction rates have been obtained for older patients as for younger ones. Focusing on the efficacy of HT may mask the efficacy of CT. This finding suggests that the problem mainly involves physicians’ representations. Lastly, our results suggest that some halo effect or anchoring effect may have occurred, since there was a general tendency to associate elderly patients with their co-morbidities and therefore to assimilate them with patients with a lower tolerance to treatment. This assumption was supported by the negative impact on CT prescription of being a medical oncologist from a CCC (these practitioners necessary compared elderly patients to the whole population of cancer patients), and having had the oldest patient (A2) as the first clinical case presented (elderly patients became the reference frame [36]). One of the conclusions to be drawn from this study, as stated by the great majority of the sample, is the need of randomized clinical trials, specifically dedicated to this population, to improve evidence based medicine about optimal chemotherapy regimens, dose and schedule [38] and to obtained results in term of disease free and overall survival according to physiological versus chronological age. Another proposition could be a greater specialization in onco-geriatrics to improve physicians’ ability to identify elderly patients and prevent elderly patients from being regarded a priori as having a lower tolerance to treatment than other cancer patients. Or at least, as already suggested [38], [39], [40], effort have to be made to facilitate a closely collaboration between oncologists and geriatricians, for example with the systematic presence of a geriatrician during medical staff. Another point which requires to be investigated more thoroughly is elderly cancer patients’ own point of view and their wishes about their own treatment and the care process [41], in particular knowing majority of colorectal cancer patients surveyed by Elkin et al. [42] had decided to receive chemotherapy. Given the multiple factors and risks involved in the care process with this specific population, patients’ preferences should be elicited and taken into account. Conflict of interest There is no conflict of interest from each of the authors in term of financial or personal relationships with other people or organizations that could have inappropriately influenced this work. Reviewers Professor Margot Gosney, University of Reading, Institute of Health Sciences, Building 22, London Road, Reading, RG1 5AQ, United Kingdom. Dr. Arash Naeim, Assistant Professor of Medicine, David Geffen School of Med., Univ of California, Division of Hematology-Oncology, 10945 Le Conte Avenue, Suite 2345, Box 951687, Los Angeles, CA 90095-1687, United States. Acknowledgments A particular acknowledgement to Anne Chantal BRAUD† for her participation in the conception of the design of the questionnaire. We also thank two anonymous reviewers for their comments that helped to improve the manuscript. This survey was supported by the French National Federation of Cancer Centers (FNCLCC), the National Institute of Health and Medical Research (INSERM), and the French Society of Private Cancerology, who authorized us to use their logo on the explanatory letter that was sent out with the questionnaire. Financial support was provided by the French Foundation (Fondation de France). Appendix A. Clinical case AA 55/76-year-old patient without any antecedents undergoing treatment for AHT, excellent general status. KI: 90%, lives with her husband. Tumorectomy performed two weeks previously, diameter 40mm, HR+, SBR 2, peritumoral embolies+, 3N+ on 10. Patient's HER 2 status not known, healthy margin at 10mm, normal cardiac scan. Clinical case BA 78-year-old patient undergoing treatment for AHT, with non-insulin-dependent diabetes treated and equilibrated, normal cardiac scan, good health status KI 70%, living alone. Tumorectomy performed two weeks previously, diameter 30mm, SBR3, HR-, no peritumoral embolies, 1N+ on 6, negative extensive staging, healthy margin at 15mm, normal cardiac scan. Clinical case CA 71-year-old patient with good general health status, KI 80%, living alone. Tumorectomy performed two weeks previously, diameter 30mm, SBRIII, HR+, no peritumoral embolies, 2N+ on 8, negative extensive staging, healthy margin at 15mm, normal cardiac scan. Clinical case DA 55-year-old menopausal patient undergoing treatment for AHT, good general health status, KI 100%, overweight, married with no children. Tumorectomy performed two weeks previously, diameter 20mm, SBR1, HR+, no peritumoral embolies, 2N+ on 15, negative extensive staging, healthy margin at 10mm, normal cardiac scan. For each clinical case, the questions asked to the physicians were as follows: Appendix B. In terms of overall survival, irrespective of the chemotherapy regimen chosen, a combination of chemotherapy and hormonotherapy resulted in the same proportional risk reduction for case D as for case A1 (reference case used for comparisons). For cases A2 and C, the proportional risk reduction associated with a combined adjuvant treatment was slightly lower but quite similar to that obtained in case A1. With case C, chemotherapy resulted in the same proportional risk reduction as in case A1. 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C. Protière received her Ph.D. in economics from the University of Mediterranean. She is currently a researcher in health economics in the research unit 912 SE4S “Economy & Social Sciences, Health Care Systems & Societies” INSERM – IRD – University of the Mediterranean. Her scientific work focuses on patient physician relationship, individual and collective decisions and preferences elicitation. a INSERM, U-912 “Economic & Social Sciences, Health Systems & Societies” (SE4S), Marseille, F-13273, France b Université Aix Marseille, IRD, Marseille, F-13007, France c Université Aix Marseille, Faculté de Médecine, Marseille, F-13007, France d Institut Paoli-Calmettes, Marseille, F-13273, France  Corresponding author at: INSERM, UMR 912 “Economic & Social Sciences, Health Systems & Societies” (SE4S), 23, rue Stanislas Torrents, ORS PACA, 13006 Marseille, France. Tel.: +33 4 91 59 89 16; fax: +33 4 91 59 89 24.
PII: S1040-8428(09)00197-8 doi:10.1016/j.critrevonc.2009.09.007 © 2009 Elsevier Ireland Ltd. All rights reserved. | |
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