Affiliations of authors: S. R. Galper, J. R. Harris, Department of Radiation Oncology, Brigham and Women's Hospital, Boston, MA, and Department of Radiation Oncology, Dana-Farber Cancer Institute, Boston; S. J. Lee, Department of Biostatistics, Dana-Farber Cancer Institute; M. L. Tao, University of California at Los Angeles School of Medicine; S. Troyan, Department of Surgery, Beth Israel Deaconess Medical Center, Boston; C. M. Kaelin, Department of Surgery, Brigham and Women's Hospital, and Department of Surgery, Dana-Farber Cancer Institute; J. C. Weeks, Department of Adult Oncology, Dana-Farber Cancer Institute.
Correspondence to: Jane C. Weeks, M.D., Department of Adult Oncology, Dana-Farber Cancer Institute, 44 Binney St., Boston, MA 02115 (e-mail: jane_weeks{at}dfci.harvard.edu).
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ABSTRACT |
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INTRODUCTION |
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One of the potential benefits of ALND is its direct effect in controlling disease. ALND has been shown to decrease the rate of axillary recurrence of cancer from 18% to 1.4%, without affecting patient survival (12). Lymph node irradiation offers a reasonable alternative to ALND in preventing axillary recurrence, with several studies finding lymph node failure rates of less than 3% after treatment with tangential radiotherapy (with or without lymph node irradiation) (912).
Until recently, the most important benefit of ALND was the prognostic information it provided for use in decision making about systemic therapy. Now that adjuvant therapy is routinely offered to women who have tumors at least 1 cm in diameter regardless of lymph node status, the results of ALND are likely to alter treatment recommendations in only selected subsets of women. These groups include women with small tumors who are found at dissection to have positive axillary lymph nodes (13,14), women with many involved lymph nodes who may be candidates for more aggressive therapy and women with tumors larger than 1 cm who would choose to forego adjuvant therapy if and only if they knew their lymph nodes were negative. In these groups, it is possible that ALND could indirectly result in prolonged survival through its impact on the choice of systemic adjuvant therapy. Finally, for some women, there may also be some psychologic benefit from the prognostic information provided by lymph node dissection, even if this information does not affect management of the disease.
The benefits of ALND may come at the cost of morbidity. The most common problems experienced by patients after ALND include pain and diminished grip strength (15). Overall rates of arm dysfunction 1 year after ALND are approximately 40% in the most carefully conducted studies (1527). Moreover, the recovery of arm function following ALND may be particularly difficult for older women (28,29).
Currently, physicians weigh the risks and benefits of ALND to determine whether to perform this procedure in a given patient. If women's preferences about these factors vary, then it may be important to tailor clinical decisions about management of the axilla to the preferences of the individual patient rather than adopting a uniform treatment policy (3032).
The goal of this study was to learn more about patients' preferences regarding the trade-offs between the risks and benefits of ALND. We surveyed women with and at risk of invasive breast cancer to determine 1) if women place sufficient value on the benefits of ALND to justify the risks and 2) whether assessment of these trade-offs varies substantially among women.
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SUBJECTS AND METHODS |
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We measured the preferences of two groups of women. The first group consisted of 82 women with invasive breast cancer who had already undergone ALND and had, therefore, already made a decision about treatment to the axilla. Eligible subjects in this group were women with stage I and II breast cancer who had completed treatment with breast-conserving therapy at least 6 weeks prior to enrollment in the study. These subjects were asked to consider hypothetical scenarios that weighed the risks and benefits of ALND for newly diagnosed invasive breast cancer. The second group consisted of 62 women at risk of invasive breast cancer by virtue of a prior diagnosis of ductal carcinoma in situ (DCIS). Women in this group could have been treated with either breast-conserving therapy or mastectomy but could not have undergone ALND. We asked this second group of women to consider the same hypothetical scenarios about the treatment they might choose if they were to develop invasive breast cancer. All subjects were required to be proficient in spoken and written English.
Eligible subjects were identified from a comprehensive database of all patients treated at the Joint Center for Radiation Therapy, Harvard Medical School, from 1968 to the present. Patients were selected at random from follow-up appointment lists at Brigham and Women's Hospital, Dana-Farber Cancer Institute, Beth Israel Hospital, New England Deaconess Hospital, Massachusetts General Hospital (all in Boston, MA), and Framingham Metro West Medical Center (Framingham, MA). We sent an introductory letter describing the study to all patients scheduled for a routine follow-up appointment. Subjects who were not interested in participating returned an opt-out card. Women who did not return an opt-out card and whose appointments were scheduled at times when the interviewer was available were contacted by telephone prior to their follow-up appointment and asked to participate in the study. All patients contacted agreed to participate. One interviewer conducted all of the interviews at the time of each woman's clinic visit. The Institutional Review Boards of Brigham and Women's Hospital, Dana-Farber Cancer Institute, Beth Israel Hospital, New England Deaconess Hospital, Massachusetts General Hospital, and Framingham Metro West Medical Center approved this study. All patients gave verbal informed consent.
Data Collection
The interview began with the presentation of hypothetical scenarios that were designed to assess a woman's preferences for four potential benefits of ALND: 1) local control of the disease, 2) survival, 3) the impact of information obtained from ALND on treatment recommendations, and 4) the prognostic information obtained from ALND independent of its effect on treatment recommendations (see the "Appendix" section for an example of one such scenario). Subjects were asked to weigh each of these potential benefits of ALND against the risk of arm dysfunction. Identical versions of the hypothetical scenarios were presented to both groups of patients. All four scenarios asked subjects to imagine that they had never had a prior breast cancer diagnosis, that they had been just diagnosed with invasive breast cancer, and that the hypothetical invasive breast cancer did not represent a recurrence of the subject's initial disease. Women in the DCIS group were asked to consider the potential benefits of ALND in the context of this hypothetical scenario and not for the management of DCIS.
In the first scenario, subjects were asked to trade-off the benefit of local control against the risk of arm dysfunction. Subjects were told to imagine that they had just been diagnosed with invasive breast cancer and that they were deciding how to manage the axillary lymph nodes. The side effects of ALND were described; these included a 40% risk of mild upper-arm dysfunction that ranged in severity from minor arm numbness to impairment of activities of daily living. Subjects were asked whether they would undergo ALND assuming a 40% fixed risk of upper-arm dysfunction if ALND resulted in a given level of local control of the cancer. This level was varied in a series of iterative questions using a ping-ponging technique. The magnitude of benefit in local control at which the subject was indifferent between ALND and no ALND was considered that subject's threshold benefit level (see the "Appendix" section). In the second and third scenarios, subjects were asked to trade-off the benefits of survival and impact of information obtained at ALND on treatment recommendations, respectively, against the risk of mild upper-arm dysfunction. In the final scenario, the value of prognostic information from ALND that would not alter treatment recommendations was measured by asking women to indicate the maximum risk of arm dysfunction they would accept with ALND to obtain prognostic information. At the conclusion of each of the scenarios, subjects were asked to explain the factors motivating their responses to ensure that they had understood the intended meaning of the scenarios.
Subjects were also asked to complete a self-administered, disease-specific quality-of-life questionnaire that included constructed items and the Breast Cancer Fear of Recurrence Scale of Lasry et al. (33). Subjects with a history of invasive breast cancer and ALND underwent a direct examination of upper-arm function in both the dissected and undissected arms. The undissected arm served as a reference or control for comparison with the dissected arm. The examination included a measurement of arm circumference 10 cm above the olecranon process, a direct evaluation of passive strength, an assessment of active strength using a dynamometer, and a range-of-motion test using a goniometer. Clinical data, including age, time since diagnosis, type of surgery (mastectomy or breast-conserving surgery), and radiation therapy, were abstracted from medical charts. For patients with invasive breast cancer, the number of lymph nodes removed, the number of lymph nodes involved with the tumor, the use of axillary radiation therapy, the use and timing of chemotherapy, and the use of adjuvant tamoxifen were recorded.
Scenario Development
A multidisciplinary team of medical, surgical, and radiation oncologists designed the scenarios used in the survey. The scenarios were pilot tested on 10 breast cancer patients and on 15 female members of the administrative support staff at three Harvard-affiliated departments of radiation oncology. The scenarios were modified in response to open-ended discussions with the test subjects to ensure that the scenarios clearly represented the intended clinical situation. The readability index of the scenarios was established using a computer program (Rightwriter version 5.0; www.wiu.edu/users/miac/retired/ritewrter.htm) that determined that the written scenarios conformed to an 11th-grade reading level.
Comparisons With the Literature
To determine whether the levels of benefit patients might want before favoring ALND were within the range of what the procedure can actually deliver, we performed a literature review to estimate the absolute level of benefit provided by ALND for each of the four benefits assessed. The literature-based estimate of absolute benefit provided by ALND was used to divide our sample into two groups: 1) those for whom this benefit would be sufficient to justify the procedure and 2) those for whom it would not.
Tests of Reliability and Validity
To ensure that the subjects comprehended the content of the scenarios and the quantitative levels of risk and benefit associated with ALND, we asked them to explain the factors that motivated their responses at the completion of each scenario. These discussions suggested that the subjects had understood each scenario, including the conceptual task involved in identifying a threshold level of benefit and the meaning of the quantitative data presented. To further assess comprehension, the interviewer presented each subject with a randomly selected scenario for a second time at the conclusion of the interview. The correlation between the threshold benefit elicited from subjects on initial presentation of the scenario and subsequent representation of the same scenario was .82.
Statistical Methods
Descriptive statistics (such as median and range) were used to characterize the responses to each hypothetical scenario obtained from the two groups of subjects. Exact 95% confidence intervals (CIs) were provided for the estimated proportions. Univariate differences between categorical variables were evaluated using Fisher's exact test (34), and univariate differences between continuous variables were evaluated using the Wilcoxon rank-sum test (35). Univariate analyses were conducted to determine the impact of sociodemographic, clinical, and psychosocial factors and the presence of perceived or actual upper-arm dysfunction on preferences for ALND in each group. Each variable was dichotomized using the median value. Fisher's exact test (34) was used to assess associations. Two-sided P values are reported for all tests. Statistical tests were performed using the SAS program (Version 6.12; SAS Institute, Cary, NC).
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RESULTS |
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Characteristics of the study subjects are shown in Table 1. In both groups, the majority of subjects were white, married with children, employed, and college graduates with annual incomes of at least $42 000. These characteristics reflect the demographics of the patients treated at our institutions. The only significant difference between the two groups of subjects was the time since diagnosis (P = .001).
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Patient preferences for ALND are summarized in Table 2. When presented with an estimated local control rate of 85% in the absence of axillary therapy, the invasive cancer group required a 5% median increase in local control before they would opt for ALND. In contrast, women in the DCIS group required a 15% median increase in local control. Given a 70% chance of survival without ALND, the invasive cancer cohort required a 3% median increase in survival before they would choose this procedure, while the DCIS group required a 10% median increase in survival. Forty-eight percent of the invasive cancer group and 24% of the DCIS group would choose ALND if it resulted in a 1% improvement in survival. Subjects in the invasive cancer group required a 1% probability that lymph node dissection would alter treatment recommendations, while women in the DCIS group required a 25% probability that ALND would alter treatment recommendations. The differences in responses between the invasive cancer and DCIS groups in each of these scenarios were statistically significant (P<.001).
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Determinants of Patient Preferences
As shown in Table 2, there was considerable variability between patients in the preferences elicited for all scenarios. None of the clinical, sociodemographic, or psychosocial factors examined, including age, stage, lymph node status, treatment with radiotherapy, treatment with chemotherapy, treatment with tamoxifen, time since diagnosis, marital status, race, education, income, and fear of recurrence, consistently explained more than 5% of the variability in preferences across all four scenarios. It should be noted, however, that the true impact of race, income, or education could not be assessed in this relatively homogeneous sample. For subjects with invasive breast cancer who had undergone ALND, neither the presence of perceived upper-arm dysfunction nor the presence of actual upper-arm dysfunction predicted more than 5% of the variability in preferences evaluated by all four scenarios.
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DISCUSSION |
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Although we found that subjects valued the potential benefits of ALND, our data also show that they did not discount the risks associated with the procedure. It is striking that the majority of women in both groups found potential long-term morbidity from ALND to be a sufficiently serious concern and they were willing to accept some compromise in survival to avoid it. This finding suggests that, for some women, axillary radiation therapy, which offers excellent local control, perhaps with less long-term morbidity, may be an appealing alternative to ALND. Although subjects required substantial improvements in survival to accept a 40% risk of arm dysfunction, women in both cohorts were willing to incur even higher rates of arm dysfunction in exchange for prognostic information. These results indicate that many women place a very high value on the prognostic information provided by ALND, which is a benefit not offered by axillary radiation therapy. Women would opt for ALND, not because they are unconcerned about the side effects, but because they are willing to endure them to obtain prognostic information. If sentinel lymph node biopsy proves to provide prognostic information that is as accurate as ALND but with less morbidity, women with early breast cancer may no longer have to accept this compromise.
It is a standard maxim in medical training that one should not do a test if one would not act on the results. However, a growing body of literature demonstrates that patients may place a high value on information and may be willing to accept considerable risk to obtain it, even if the information would not change their treatment (36,37). For example, Berwick and Weinstein (36) found that pregnant women valued the information obtained from fetal ultrasound for its own sake, "seeing an image of the fetus, being reassured that the baby is normal," independent of its value for medical or nonmedical decision making. Our data indicate that women with early-stage breast cancer may attach similar value to prognostic information obtained from ALND. Of interest, in the invasive cancer group, even women who were lymph node positive mentioned that it was comforting to know the status of their axillary lymph nodes, suggesting that prognostic information may be valued even when it is not reassuring.
Several limitations of this study design should be noted. First, one could argue that the ideal study population would be women recently diagnosed with early-stage invasive breast cancer who had been educated about the various options for management of the axilla but had not yet made a treatment decision. However, we believed that it would be unethical to subject women who were in the process of making actual clinical decisions to an interview presenting an array of hypothetical outcomes, many of which might not be clinically realistic. Therefore, in this exploratory study, we chose two groups of women who could provide useful insights into the nature of preferences regarding ALND but for whom this particular study would not interfere with their care. The first group, women with a history of invasive breast cancer and treatment with ALND, were chosen because they are the real experts on what it is like to experience the actual sequelae of ALND and to realize the potential benefits of the procedure. However, this group of patients is also likely to be biased in favor of a procedure that was recommended to them and that they have already undergone. The second group of subjects, women with a history of DCIS treated without ALND, was chosen as a particularly informative group of women who are at risk of invasive breast cancer. These patients understand what it is like to face a breast cancer diagnosis, may well have considered the treatment choices they might make if faced with a diagnosis of invasive breast cancer, and have no reason to be biased for or against ALND. They might be expected to place somewhat less value on the potential benefits of ALND, however, than women newly diagnosed with invasive disease who are actually facing complex decisions about adjuvant therapy. It, therefore, seems likely that the preferences of a population of women with newly diagnosed invasive breast cancer might lie somewhere between the preferences of the two cohorts of women surveyed in this study.
Because our goal was to determine how women valued each of the specific benefits of ALND, our methods did not allow us to determine the proportion of women who would opt for ALND, all things considered, given the known levels of risk and benefit. The proportion of women for whom one or more benefits, considered independently, were sufficient to justify the risks of the procedure, the majority of our sample, provides a lower bound for this estimate however. Finally, this study was conducted in a single network of affiliated academic hospitals. The subjects were predominantly white, upper middle class, highly educated, married, and employed. Our findings cannot, therefore, be assumed to represent the views of all women with breast cancer. In our cohort, there was no consistent association between sociodemographic factors and preferences. However, we were not able to fully explore these relationships because of the relative homogeneity of our sample, and future studies in different settings and populations are clearly needed.
While most women in our study placed sufficient value on the benefits of ALND to justify the risks, not all did. Furthermore, it was not possible to predict an individual woman's preferences from her clinical or sociodemographic characteristics. This observation is consistent with prior studies of preferences showing that values for the outcomes of medical therapies are highly individualistic, tend to be stable over time, and cannot be predicted from a sociodemographic profile (3840). These findings suggest that, if the preferences of individual patients are to be honored, physicians must engage in an interactive dialogue with patients. Promising new tools designed to help facilitate shared decision making, such as interactive videodisks (41) and decision boards (42,43), have been used successfully to assist breast cancer patients with choices about surgery and adjuvant therapy. Our results suggest that management of the axilla should be added to the list of decisions for which patients' preferences should be elicited and honored.
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APPENDIX: SAMPLE SCENARIO (LOCAL CONTROL) |
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Imagine that you have discovered a small lump in your breast and have undergone a biopsy confirming the diagnosis of breast cancer. You have undergone a physical examination of the area under your arm as well as several other tests that indicate that the breast cancer is confined to your breast. You are given the choice of mastectomy versus "breast-conserving therapy" that consists of lumpectomy, i.e., removal of the lump only followed by radiation therapy to the breast. You choose breast-conserving therapy. Although the lymph nodes under your arm do not appear to be involved by physical examination, there is up to a 30% chance of tumor being there. You are now discussing with your physician how best to manage the lymph nodes under your arm.
If you had surgery to the area under your arm (axillary dissection), you would experience pain under your arm for 24 weeks after surgery. The pain might interfere with your ability to drive, exercise, and participate in sports. The pain would lessen over time. There would be a 40% chance of having some residual difficulties persisting 1 year after surgery. Upper-arm difficulties could include one or more of the following: loss of sensation in your underarm area that would improve with time, decreased range of motion of the shoulder (12%) or stiffness (5%), swelling (9%) ranging in severity from barely noticeable to more extensive impairment, pain (16%), and reduced grip strength (16%). This could reduce your physical abilities causing difficulties with reaching, lifting, pushing, or prolonged repetitive activities, such as typing or knitting. In rare cases (<1%), you may require assistance with daily activities, such as dressing, housekeeping, shopping, meal preparation, and transportation. If you did not have the axillary surgery, it is unlikely that you would experience any change in your arm function from what you are presently able to do.
As difficult as it may be to comprehend, assume for the purposes of this scenario that this surgery, axillary dissection, would not improve your chances of surviving this breast cancer. That is, you are just as likely to survive the same amount of time with or without this surgery.
Having the surgery, however, would reduce the chances of the breast cancer eventually becoming apparent under your arm. There would be a 1% chance that the tumor would appear under your arm following axillary surgery. If you did not have the axillary surgery, there is a higher chance that the tumor would appear under your arm in the future. If the tumor subsequently appeared under your arm, you could receive additional therapies (surgery, radiation therapy, and/or chemotherapy) that would control the tumor. The tumor appearing under your arm does not mean that the cancer has spread elsewhere or that you will die of it. With treatment of the axilla at the time of recurrence, there would be a 40% chance of some residual difficulties, the same as if you underwent axillary surgery at the time of diagnosis of breast cancer.
Assume for the purpose of this scenario that recommendations on chemotherapy will be made on the basis of the information from the lumpectomy alone and not the axillary surgery.
Remember, this is only an imaginary situation, and the events that I am describing will not necessarily happen to you. This information is only being presented for our study purposes to measure women's preferences about surgery to the lymph nodes under the arm.
In summary, having surgery means that there is only a 1% chance of the tumor appearing under your arm in the future. There is a 40% chance that long-term arm dysfunction, as described above, would occur after the surgery. If you did not have surgery to the lymph glands under your arm, there is up to an 85% chance that tumor would never appear under your arm in the future. If tumor did appear under your arm in the future, it could be controlled with other therapies. If you did not have surgery to the lymph glands under your arm, it is unlikely that you would have any change in arm function.
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NOTES |
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Manuscript received March 15, 2000; revised August 10, 2000; accepted August 23, 2000.
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