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Adjuvant Tamoxifen Prescription in Women 65 Years and Older With Primary Breast Cancer

From the Department of Medicine, Boston University School of Medicine, Department of Epidemiology and Biostatistics, Boston University School of Public Health, and Department of Health Care Policy, Harvard Medical School, Boston, and Meyers Primary Care Institute, Fallon Healthcare System and the University of Massachusetts School of Medicine, Worcester, MA; Department of Community Health, Brown University, Providence, RI; University of California Los Angeles Schools of Medicine and Public Health, Los Angeles, CA; and Healthcare Education and Research Foundation, Inc, St. Paul, MN.

Address reprint requests to Rebecca A. Silliman, MD, PhD, Boston Medical Center, 88 East Newton St, F4, Boston, MA 02118; email: rsillima{at}bu.edu

	ABSTRACT

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PURPOSE: We examined patterns of adjuvant tamoxifen discussion and prescription among breast cancer patients age 65 years and older.

METHODS: We selected from women diagnosed with primary breast cancer those with (1) stage I (tumor diameter 1 cm), stage II, or stage IIIa disease; (2) age 65 years or older on the date of diagnosis; and (3) permission from the attending physician to contact. Data were collected from consenting patients’ medical records, telephone interviews with patients, and mailed questionnaires completed by their physicians.

RESULTS: We obtained medical record and interview data for 698 patients. The oldest patients (odds ratio [OR], 0.45; 95% confidence interval [CI], 0.23 to 0.87 for those aged 80+ relative to those aged 65 to 69 years old), those with more comorbid conditions (each additional comorbid condition reduced the odds of discussion by 0.84; 95% CI, 0.73 to 0.96), and those who were estrogen receptor–negative (OR, 0.56; 95% CI, 0.32 to 0.99) were less likely to report discussion of tamoxifen therapy with a physician. Older patients (OR, 2.17; 95% CI, 1.18 to 4.01 for 70- to 79-year-olds relative to 65- to 69-year-olds; OR, 2.44; 95% CI, 1.11 to 5.34 for those aged 80+ relative to those aged 65 to 69 years old), those who reported a greater influence of information about tamoxifen on decision-making (an increase in 1 SD increased the odds by 7.43; 95% CI, 4.36 to 12.65), and those whose physicians believed that the benefits of tamoxifen outweighed its risks (an increase in 1 SD increased the odds by 1.87; 95% CI, 1.34 to 2.62) were more likely to be prescribed tamoxifen.

CONCLUSION: These findings highlight the key role of communication in the care of older women with breast cancer and its ultimate influence on the receipt of therapy.

	INTRODUCTION

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THE RECENT NATIONAL Institutes of Health consensus panel wrote "adjuvant hormonal therapy should be recommended to women whose breast tumors contain estrogen-receptor protein, regardless of age, menopausal status, involvement of axillary nodes, or tumor size."¹ The two possible exceptions were premenopausal women with small tumors (< 10 mm in diameter) and elderly women with similarly small tumors plus a history of thromboembolic disease.¹ Moreover, the 2001 St Gallen Sixth International Consensus Panel recommended that, with the exception of low-risk node-negative patients and those who are estrogen receptor–negative, all postmenopausal women with breast cancer receive 5 years of tamoxifen therapy.²

A substantial number of studies have demonstrated that older women are less likely than younger women to receive appropriate care for a new diagnosis of breast cancer.^3-17 These age-dependent variations have persisted into the 1990s, although they are reflected mostly in primary tumor therapy.^14-17 The relationship between age and systemic adjuvant therapy has been investigated less extensively. In a study of postmenopausal women 50 years of age, Guadagnoli et al¹⁸ found that treatment with hormonal therapy decreased with age. In contrast, hormonal therapy increased with age among node-positive women, reaching a maximum of 68% among women 70 to 79 years of age. Lower use among younger women reflected greater use of chemotherapy, so overall use of adjuvant therapy did not vary according to age among node-positive women (92% across age groups).¹⁸ Using coarser age categorizations (50 to 69 v 70+ years of age), Hebert-Croteau et al¹⁶ found little variation in the use of systemic adjuvant therapy (tamoxifen, chemotherapy, or both) as a function of age. The proportion of stage I patients receiving systemic adjuvant therapy was also similar in both age groups, but younger women with stage II disease were more likely to receive adjuvant therapy than were their older counterparts (72.3% v 64.1%, respectively). Tamoxifen therapy was similar in both groups, but chemotherapy was more likely in the younger group.

Investigations of the reasons for variations in breast cancer care have evaluated the roles of patients’ health status,^4,6,9,14-17 patients’ and families’ preferences and support,^15,19,20 physicians’ attitudes and beliefs,^6,21,22 and patient-physician communication.^14,23 In a study of women 55 years of age diagnosed with early-stage breast cancer, we found that surgeon sex is independently associated with the receipt of both primary tumor therapy and systemic adjuvant therapy.²⁴ Furthermore, patients who have better perceptions of their abilities to discuss treatment options and who see more breast cancer physicians at the time of primary diagnosis are more likely to be treated with tamoxifen.²⁵

In a cohort of women 65 years and older with early-stage breast cancer diagnosed from 1996 to 1999, we sought to characterize patterns of tamoxifen prescription and to determine whether doctor-patient communication—measured more comprehensively from the perspective of both doctor and patient—influenced tamoxifen prescription. Specifically, we sought to identify patient and physician factors associated with (1) patients’ reports of discussing tamoxifen therapy with a physician, and (2) the prescription of tamoxifen.

	METHODS

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Sampling
We identified women diagnosed with primary breast cancer between December 1, 1996, and September 30, 1999, in 12 hospitals in Rhode Island, one hospital in southeastern Massachusetts, 18 hospitals in North Carolina, 23 hospitals in Minnesota, and eight hospitals in Los Angeles. We identified women through regular review of pathology reports at hospitals or collaborating tumor registries and selected women with (1) stage I disease and a tumor diameter of 1 cm or greater, stage II, or stage IIIa disease; (2) age 65 years or older on the date of diagnosis; and (3) permission from the attending physician to be contacted for study participation.

Once permission for patient contact was obtained, the following additional entry criteria were applied: (1) no prior history of primary breast cancer, (2) no simultaneously diagnosed or treated second primary tumor at another site, (3) English speaking or with an available translator, and (4) competent for interview with satisfactory hearing or with an available proxy respondent. Eligible participants were mailed an enrollment package and were called by project personnel who explained the study’s purpose and participation requirements and who requested participation in the study. We excluded women who declined to participate or who were not enrolled within 5 months of the date of their most definitive primary breast cancer surgery. Participation in clinical trials did not preclude study enrollment. Women who agreed to participate were asked to return a signed consent form approved by the institutional review board associated with the hospital from which she was identified. Eligible participants were given the option of full study participation (medical record review and three telephone interviews) or limited participation (medical record review only).

Surgeons and medical oncologists of participating patients were mailed an enrollment package that contained an introductory letter, a one-page summary of the study’s methods and objectives, a consent form, and a baseline questionnaire (see Data Collection). Physicians who returned signed consent forms were enrolled onto the study.

Data Collection
Enrolled participants were asked to complete three telephone interviews of 35 to 50 minutes’ duration each at 3 to 5 months, 6 to 8 months, and 15 to 17 months after the date of definitive surgery. We report in this analysis on full study participants using data collected through the second interview. We used the patient interviews to collect demographic (age, race, marital status, education, living arrangements, employment status, and annual income), health status (comorbid conditions, general and breast cancer–specific health-related quality of life), primary and systemic adjuvant therapy (receipt of radiation therapy, chemotherapy, and tamoxifen therapy), and breast cancer treatment decision-making information. Project personnel reviewed and abstracted patients’ medical records at least 3 months after the date of definitive surgery to collect information about tumor characteristics (size, node status, histologic and nuclear grade, and estrogen/progesterone receptor status), treatments received, and comorbid conditions.

The patient’s surgeon completed a patient-specific treatment recommendation form after receipt of the patient’s written informed consent. The patient’s medical oncologist completed a similar form if the patient had been referred. The treatment recommendation form asked physicians to provide an overall assessment of the patient’s health at presentation, to judge the importance of factors that influenced their decision-making regarding tamoxifen prescription, and to estimate the patient’s prognosis with and without a course of tamoxifen therapy.

All physicians were asked to complete a baseline questionnaire that collected sociodemographic characteristics (age, sex, race, and marital status), professional characteristics (specialty and year of graduation from medical school), and practice characteristics (number of breast cancer patients cared for per year, size of primary hospital, and affiliation with a medical school). When key data elements were missing, we obtained them from American Medical Association databases.²⁶

Analytic Variables
For most variables, we used data from the baseline instruments to construct our analytic variables. We altered this strategy when patient interview responses might have been influenced by the temporal sequencing of therapies: the receipt of systemic adjuvant chemotherapy, factors influencing patients’ decision-making regarding tamoxifen treatment, patients’ reports of discussing tamoxifen treatment with their physicians, and prescription of tamoxifen. If any of these data elements were missing in the baseline interview but were present in the first follow-up interview, we used the relevant responses from the first follow-up interview. Similarly, if the patient answered "no" to the discussion and prescription variables at baseline but answered "yes" in the first follow-up interview, we obtained all of these data elements from the first follow-up interview data.

Independent Variables
Patient characteristics. We classified patient age as 65 to 70 years, 70 to 79 years, or 80+ years. Our measure of physical function was the PFI10 (scaled from 0 to 100, with higher scores reflecting better function) from the Medical Outcomes Study 36-Item Short Form.²⁷ A count of comorbid conditions present at the time of breast cancer diagnosis was determined by medical record review using the Index of Coexistent Diseases.²⁸ Examples of specific diseases include ischemic heart disease, congestive heart failure, cerebrovascular disease, diabetes mellitus, and chronic obstructive pulmonary disease.

Tumor characteristics. We classified tumor, node, metastasis stage as I, IIa, IIb, or IIIa, on the basis of measures of tumor size and axillary node status. When axillary node dissection was not performed, axillary node status was determined on the basis of clinical examination. Estrogen receptor status was categorized as positive, negative, or indeterminate.

Primary tumor therapy. We classified patients as receiving a mastectomy, breast-conserving surgery (BCS) followed by radiation therapy, or BCS alone. We also documented the form of axillary node evaluation information as through axillary node dissection, sentinel-node biopsy, or both.

Systemic adjuvant chemotherapy. In both interviews, we asked whether patients had received chemotherapy.

Factors influencing patients’ decision-making regarding tamoxifen treatment. Women rated the influence of 11 factors associated with their decision-making about treatment with tamoxifen. Items were generated by the investigative team and were pilot tested by five older women who had participated in a prior study.¹⁴ Items included in this measure (Information Influence) are displayed in the upper portion of the Appendix. Responses were coded according to four categories from "very influential" to "not influential at all." A "don’t know" response was considered as "not influential at all." We then determined whether each factor was influential (yes = very or somewhat influential, no = all other responses) and calculated the percentage of responses considered influential.

Factors influencing physicians’ decisions regarding tamoxifen treatment. We asked physicians to rate the importance of 11 factors regarding their decision to recommend or not to recommend adjuvant tamoxifen therapy. Where possible, the content of items was similar to that of the items we asked patients. Before fielding, items were pilot tested by two surgeons and two medical oncologists.

If both a surgeon and a medical oncologist completed forms for a particular patient, we used the medical oncologist’s form. Ratings on each of the 11 items ranged from "very important" to "very unimportant." These items were used to create scores related to the benefits (the pros) and the risks (the cons) of recommending tamoxifen for a particular patient. The transtheoretical model of behavior change²⁹ suggests that when the pros are higher than the cons, a positive behavior (recommending tamoxifen) results, and vice versa. In our analysis, we expected prescription of tamoxifen for a particular patient to be more likely when her physician’s pro score outweighed the con score and to be less likely when the con score outweighed the pro score.

Consistent with the transtheoretical model, principal component analysis of the 11 items revealed two distinct factors representing the pros and cons for recommending tamoxifen. Five items constituted the pro score (coefficient alpha = .79) and six items constituted the con score (coefficient alpha = .75). We used these scores to create a physician decisional balance score (pro score minus con score) for each patient. Items included in this measure are displayed in the lower portion of the Appendix.

Dependent Variables
Physician discussion of adjuvant tamoxifen. We asked patients whether their surgeons, and medical oncologists if referred, had discussed adjuvant tamoxifen therapy with them. If patients reported that either their surgeon, their medical oncologist, or both had discussed adjuvant tamoxifen therapy with them, discussion of tamoxifen therapy was classified as "yes"; otherwise, it was classified as "no."

Prescription of adjuvant tamoxifen. In the baseline interview and first follow-up interview, we asked patients whether tamoxifen was prescribed. If a patient responded "don’t know" to this question, we coded it as "no." To address the validity of self-report of tamoxifen prescription, we studied a subset of patients (n = 45) who received a prescription benefit through their health maintenance organization. With a recent pharmacy filling of a tamoxifen prescription as the gold standard, self-report of tamoxifen prescription had a sensitivity of 94% and a specificity of 91%, with an overall error rate of 7%.

Analytic Strategy
We compared the characteristics of patients for whom physicians refused permission to contact with those for whom they allowed contact, and then compared patients who refused to participate in the study with those enrolled according to age and geographic region using Pearson ² tests. Using Pearson ² tests for categorical variables and Student’s t test for continuous variables, we assessed patient and physician factors that were related to the two dependent variables. We report two-tailed P values for these descriptive analyses.

To identify factors associated with each of the two outcome variables of interest, we created two logistic regression models. Each model included the patient’s age (70 to 79, or 80+ v 65 to 70 years), region (Rhode Island, Minnesota, or North Carolina v Los Angeles), stage (IIa, IIb, or IIIa v stage I), primary therapy (BCS plus radiation therapy or BCS alone v mastectomy), estrogen receptor status (negative or indeterminate v positive), receipt of chemotherapy, physical functioning, number of comorbid conditions, patient information influence score (only for the prescription model), and physician decisional balance score. We constructed the models using generalized estimating equations to adjust for clustering of patients within physicians.³⁰ Almost half of the 284 physicians cared for a single patient and 90% treated five or fewer. We report adjusted odds ratios and 95% confidence intervals for the significant associations in these logistic models.

Data were missing for physical functioning (1%), number of comorbid conditions (1%), and physician decisional balance score (38%). Because deleting these cases or using indicator variables for missing values in adjusted analyses could introduce biases, we used NORM statistical software to obtain multiple imputed values for respondents missing these data.³¹ The imputation model contained all variables thought to be predictive of the missing values including all variables in the multivariate regression model; the patient’s education, marital status, number living in the household, race, mental health scale from the Medical Outcomes Study 36-Item Short Form; and the physician’s specialty, sex, marital status, size of primary hospital, affiliation with a medical school, years since graduation from medical school, percentage of newly diagnosed breast cancer patients over 70 years old, and average decisional balance score across patients for whom the physician completed a patient-specific treatment form.

	RESULTS

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Sample Characteristics
Enrollment of subjects onto the study is displayed in Fig 1. We obtained permission from physicians to contact 1,621 women; 852 consented to full study participation and 81 women consented to medical record review only. The proportion of women whose physicians refused to allow them to be contacted increased as a function of age, from 16% (65 to 69 years old) to 25% (80 years and older). Similarly, the patient refusal rate increased with age, from 35% (65 to 69 years old) to 52% (80 years and older). The proportion of women who refused to participate also differed by enrollment site: North Carolina, 31%; Rhode Island, 29%; Minnesota, 40%; and Los Angeles, 63%.

View larger version (11K): [in this window] [in a new window]   Fig 1. Study enrollment and participation.

The characteristics of the enrolled sample are listed in Table 1. Each of the sites contributed approximately equal numbers of patients (data not shown). About half of the sample was between 70 and 79 years of age. Most had completed at least a high school education and most were white. About half were married. In addition, about half had stage I disease and three quarters were estrogen receptor–positive. Almost all received either a mastectomy or BCS followed by radiation therapy and almost all had an axillary node evaluation. Systemic adjuvant therapy was received by 77%, primarily tamoxifen only.

Factors Associated With Patients’ Reports of a Discussion of Tamoxifen Therapy
The oldest age group (80+ years of age), those with poorer physical function, those with more comorbid conditions, and those who were estrogen receptor–negative were less likely to report that tamoxifen therapy was discussed with them (Table 3). A higher physician decisional balance score was positively associated with the reported discussion of tamoxifen. In the multivariate model, patients aged 80+ (odds ratio [OR], 0.45; 95% confidence interval [CI], 0.23 to 0.87 relative to 65- to 69-year-olds), who had more comorbid conditions (each additional comorbid condition reduced the odds of discussion by 0.84; 95% CI, 0.73 to 0.96), and who were estrogen receptor–negative (OR, 0.56; 95% CI, 0.32 to 0.99) were less likely to report that they discussed tamoxifen therapy with a physician.

	DISCUSSION

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Among estrogen receptor–negative women, almost half did not receive any adjuvant therapy and the proportion not receiving therapy increased with age. This pattern may reflect physician uncertainty regarding efficacy and safety, because there are few clinical trial data from women 70 years of age or older.³² Although the value of chemotherapy alone, or in conjunction with tamoxifen, has not been well studied in older women, the St Gallen Panel recommends it for high-risk node-negative and node-positive women with no estrogen receptor or progesterone receptor expression.² As was emphasized by the consensus panel, there is an urgent need for the inclusion of women over the age of 70 years in chemotherapy clinical trials.¹ This remains a major clinical and research challenge, given the substantial underrepresentation of older women in breast cancer clinical trials to date.³³

To understand more fully the patterns of care observed, we considered doctor-patient communication from two perspectives. First, in our multivariate model with discussion of tamoxifen therapy with breast cancer physicians as the dependent variable, patients’ age, number of comorbid conditions, and estrogen receptor status were independently associated with the outcome. The estrogen receptor status association is in accordance with current clinical recommendations^1,2 and the age association is consistent with the reports of others who have found that older women prefer a more passive role in treatment decision-making.^34-36 However, the association between comorbid conditions and the discussion of tamoxifen was unexpected. Overall, the number of comorbid conditions documented in patients’ medical records was relatively low (Table 2) despite their advanced age. As Extermann et al³⁷ point out, even an 80-year-old woman with three comorbid conditions has an average life expectancy of 8.4 years. For such a woman, treatment with adjuvant tamoxifen would reduce the absolute risk of recurrence and mortality by more than 1%.

Although patients in the oldest age group and with more comorbid conditions were less likely to report a discussion of tamoxifen therapy, these associations did not persist in the multivariate model with prescription of tamoxifen as the dependent variable. Here we found that patients in the two older age groups were more likely to be prescribed tamoxifen, as were patients who were estrogen receptor–positive. We also found that patients who had higher information influence scores and whose physicians had higher decisional balance scores had a higher likelihood of being prescribed tamoxifen than other women. Although older women tend to agree to the therapy that their physicians recommend,^34-36 many women desire specific information about treatment risks and benefits.³⁵ This desire is consistent with our finding that women who reported that a greater number of influential factors in their decision-making were more likely to be prescribed tamoxifen. These women may have desired more specific information and, as a result, obtained it. In the case of tamoxifen, the risks of therapy are small and serious risks are rare. Thus, physician provision of more specific information about the benefits as well as the types and frequency of side effects would support the prescription of tamoxifen, particularly because the major benefit of the therapy is the reduction of risk of recurrence. When physicians’ recommendations are perceived as clear and positive, acceptance of a therapeutic option is more likely.³⁸

Whether the high levels of tamoxifen prescription that we observed will be translated into long-term adherence is not known. Fifteen percent of older women discontinue adjuvant tamoxifen by 3 years after initiation, and those who experience side effects are more likely to discontinue therapy.²⁵ Moreover, a recent study of adjuvant tamoxifen therapy during the first year after breast cancer therapy found that 30% of women with early-stage breast cancer take tamoxifen less than 80% of the time.³⁹ If the initial prescription of tamoxifen becomes more uniform, greater attention will need to be paid to quantifying the magnitude of nonadherence and discontinuation problems in clinical practice, and to identifying factors associated with them.

Although we studied recently diagnosed older female patients, including a sizable number of women 80 years of age or older, our results must be interpreted with the following limitations in mind. First, substantial selection factors resulted in a healthy, educated sample of primarily white women. It is possible that rates of adjuvant therapy discussion and prescription are lower in more diverse samples of women. Second, we relied on patients’ reports of doctor-patient communication as well as prescription of tamoxifen and chemotherapy. The former reports reflect perceptions, but it can be argued that perceptions are as important, if not more important, than what actually transpired. With respect to the accuracy of reports of tamoxifen therapy, our small validity study suggests that older women accurately report its prescription. It is unlikely that women would erroneously report that they received chemotherapy when they did not, or vice versa. Finally, our analyses are cross-sectional. Longer term follow-up of our cohort will allow us to determine the prevalence of nonadherence and the factors associated with it, including cost, side effects, and quality-of-life considerations.

APPENDIX
Information Influence Measure Some women are prescribed tamoxifen after they have had breast cancer surgery and others are not. You and your doctors made the best decision for you. I am now going to read you a list of issues that might have influenced your decision-making about treatment with tamoxifen for your breast cancer. After each issue, I will ask you to tell me whether the issue was very influential, somewhat influential, had little influence, or was not influential at all.

1. The likelihood that tamoxifen would reduce the risk of your breast cancer coming back.

2. How long you would have to take tamoxifen.

3. Side effects of tamoxifen treatment; for example, hot flashes or nausea.

4. How much tamoxifen would cost, over and above what your insurance would pay.

5. The possibility that tamoxifen would reduce your risk of problems with osteoporosis.

6. The risk of tamoxifen causing other serious problems; for example, phlebitis or endometrial cancer.

7. The likelihood that tamoxifen would reduce your risk of heart disease.

8. The likelihood that tamoxifen would reduce your risk of a new cancer in your other breast.

9. The possibility that tamoxifen would increase your risk of developing cataracts.

10. Having to make extra doctor visits to have your tamoxifen treatment monitored.

11. Hearing that the benefits of tamoxifen outweigh the risks.

Physician Decisional Balance Measure Please rate the importance of each of the following factors in your decision to recommend or not to recommend adjuvant tamoxifen therapy for this patient.

1. Treatment with tamoxifen will reduce her risk of local recurrence of her breast cancer.

2. Treatment with tamoxifen will not improve her already favorable prognosis.

3. Treatment with tamoxifen will increase her risk of developing uterine cancer.

4. Treatment with tamoxifen will increase her risk of cataracts.

5. Treatment with tamoxifen will be difficult for her to tolerate because of side effects such as hot flashes, depression, or mood swings.

6. Treatment with tamoxifen will increase her risk of thromboembolic disease.

7. Treatment with tamoxifen will reduce her risk of metastases.

8. Treatment with tamoxifen might reduce her risk of heart disease.

9. Treatment with tamoxifen will reduce her risk of developing contralateral breast cancer.

10. Treatment with tamoxifen might reduce her risk of osteoporosis.

11. Treatment with tamoxifen will be difficult for her to afford.

	ACKNOWLEDGMENTS

 
Supported by National Cancer Institute research grant no. CA/AG 70818.

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Submitted August 21, 2001; accepted March 6, 2002.

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