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Patient Beliefs and Tamoxifen Discontinuance in Older Women With Estrogen Receptor—Positive Breast Cancer

From the Boston University Medical Center, Boston MA

Address reprint requests to Rebecca A. Silliman, MD, PhD, Boston Medical Center, 88 E Newton St, Robinson 2, Boston, MA 02118; e-mail: rsillima{at}bu.edu

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION Authors’ Disclosures of... REFERENCES

 
PURPOSE: To investigate the patterns and predictors of tamoxifen discontinuance throughout a 2-year period in a cohort of women 65 years or older with newly diagnosed, estrogen receptor (ER)–positive breast cancer, focusing on the role of patients’ beliefs about the risks and benefits of tamoxifen therapy.

SUBJECTS AND METHODS: We enrolled a convenience sample of women cared for in four geographic regions of the United States with stage 1 ( 1 cm), stage II, or stage IIIA disease; no prior history of breast cancer; and no simultaneously diagnosed second primary breast cancer. Data sources included medical records and telephone interviews with patients at 3, 6, 15, and 27 months following definitive surgery.

RESULTS: Of the 597 women with ER-positive tumors, 516 women (86%) were prescribed tamoxifen, and of these, 88 (17%) stopped taking tamoxifen during the 2-year follow-up period. Of the women who stopped taking tamoxifen, the majority (68%) took it for less than 1 year. Women with neutral or negative beliefs about the value of tamoxifen (3.0; 95% CI, 1.6 to 5.6) and those with positive nodes (odds ratio = 2.5; 95% CI, 1.0 to 6.3) were more likely to discontinue tamoxifen therapy.

CONCLUSION: How women with early-stage breast cancer perceive the risks and benefits of tamoxifen therapy seems critical for sustaining adherence to adjuvant tamoxifen therapy. Interventions designed to educate women about the benefits and risks of tamoxifen therapy may help to reduce discontinuance.

	INTRODUCTION

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Five years of tamoxifen therapy reduces the risk of breast cancer recurrences by 50%, and the risk of breast cancer mortality by 28%, in woman with early-stage breast cancer who are estrogen receptor (ER)–positive.¹ Thus, current guidelines recommend 5 years of tamoxifen for all postmenopausal women with breast cancer, except women with low-risk node-negative tumors or those with ER-negative tumors.^2,3 Despite these guidelines, little is known about long-term adherence in older women who initiate adjuvant tamoxifen therapy. Randomized clinical trials of adjuvant therapy have reported 5-year discontinuance rates of 23%⁴ and 40%,⁵ and the primary prevention trial reported a 5-year discontinuance rate of 24%.⁶ However, findings from clinical trials often do not reflect what happens in clinical practice.

We previously studied tamoxifen discontinuance in women 55 years and older who were cared for in community settings, and we observed that 15% of study participants had stopped taking tamoxifen during a nearly 3-year follow-up period.⁷ In a study of persons participating in the New Jersey Medicaid or the Pharmaceutical Assistance to the Aged and Disabled programs, Partridge et al⁸ documented that 32% of women had discontinued tamoxifen by 2 years after filling their first tamoxifen prescription.

Research to date suggests that younger (< 45 years) and older ( 85 years) women, nonwhite women, those who undergo mastectomy,⁸ those with ER-negative tumors, and those who experience side effects related to tamoxifen⁷ are less likely than other women to adhere to treatment. However, the associations observed across studies have been inconsistent, perhaps in part related to the different populations studied, as well as to differences in the definition of adherence (taking or not v taking a defined minimum proportion or not). This lack of consistency reflects the general state of research related to medication adherence; researchers have been unable to develop a unifying causal model to explain medication adherence or lack thereof.⁹

Recognizing these theoretical challenges, we chose a well-developed model of behavior change, the Transtheoretical Model (TTM), to guide our study.¹⁰ Although first developed in relation to smoking cessation, the TTM has been successfully applied to such diverse behaviors as sunscreen use, exercise, and screening mammography.¹⁰ The model provides an integrated framework for focusing attention on two basic elements of behavior change: (1) stages of adoption, which are based on past and current behaviors as well as future intention; and (2) the psychological domain—the "pros" (benefits to be expected) and "cons" (risks or barriers to use) related to a behavior change. Pros and cons can be combined by subtraction into a decisional balance score. A positive score has been linked to positive actions, and a negative score, to inaction or relapse.¹⁰ Relative to adjuvant tamoxifen therapy, the TTM predicts that women with positive decisional balance scores are more likely continue therapy than women with negative decisional balance scores.

We investigated the patterns and predictors of tamoxifen discontinuance during a 2-year period in a cohort of women 65 years or older with newly diagnosed ER-positive breast cancer. We considered the role of patients’ beliefs about the risks and benefits of tamoxifen therapy, as well as a range of predictors that have been previously identified.

	SUBJECTS AND METHODS

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Study Subjects
Details of the study subjects and the data collection methods have been described.¹¹ We enrolled a cohort of women who were diagnosed with breast cancer between December 1, 1996, and September 30, 1999, in hospitals in Rhode Island, North Carolina, Minnesota, and Los Angeles, CA. We identified potentially eligible women by reviewing pathology reports at hospitals and collaborating tumor registries. Women were eligible if they were 65 years or older at diagnosis; had stage 1 ( 1 cm), stage II, or stage IIIA disease; and had no prior history of breast cancer nor a simultaneously diagnosed second primary breast cancer. We obtained permission to contact patients from their surgeons. We enrolled all women within 5 months of their most definitive breast cancer surgery and all study participants provided written informed consent using consent forms approved by associated institutional review boards.

Figure 1 displays entry into the study reported herein. We restricted our study sample to women with ER-positive tumors, since ER positivity is a major indication for tamoxifen use. We also restricted our sample to those who were both prescribed, and reported actually taking, tamoxifen, excluding those who were prescribed tamoxifen but never took the drug. In addition to being primarily interested in understanding why women who begin therapy stop it, we were concerned that those that were prescribed but never began taking tamoxifen might be quite different from those who started and stopped. Although the groups were similar with respect to sociodemographic, tumor, and treatment characteristics, they were quite different with respect to their decisional balance scores (see Analytic Variables subsection). Only 29% of those who never took tamoxifen had positive scores, whereas 73% of those who began but later stopped tamoxifen had positive scores (P = .0001).

View larger version (33K): [in this window] [in a new window]   Fig 1. Subject flow for study entry.

Dependent Variable: Discontinuation of Tamoxifen
At each interview, our study participants were asked a series of questions about tamoxifen prescription. All women were asked if they had been prescribed tamoxifen. We classified a woman as having discontinued tamoxifen at the first subsequent interview in which she reported that she was no longer taking tamoxifen, regardless of the reason for stopping.

As previously reported,¹¹ we conducted a validation of self-reported adherence among the subset of our study participants who were members of Kaiser Permanente of Southern California and for whom we had available pharmacy records. We compared the pharmacy records to our interview data and found that 89% of the women who reported that they were taking tamoxifen had supporting pharmacy documentation.

Independent Variables
Sociodemographic characteristics. We categorized women into age groups of 65 to 69, 70 to 79, and 80 years of age, and categorized education as less than high school, high school graduate, and higher education (eg, college, university). To assess adequacy of financial resources, we asked about insurance coverage for all prescription medications (some or all v none), monthly out-of-pocket expenditure for all medications ($0 to $50, > $50 to $100, and > $100), and perceived adequacy of overall financial resources (yes/no).

Health status. We ascertained each woman’s comorbidities, including the presence of heart, vascular, respiratory, liver, renal, and gastrointestinal disease; diabetes; other malignancies; and arthritis, based on the Index of Co-Existent Disease¹²; we then classified them as 0 to 1, 2, 3, and 4 comorbidities. We classified number of prescription medications, including tamoxifen, as 0 to 2, 3, 4, and 5 based on quartiles among the adherent women.

Breast cancer characteristics and treatment. We classified tumor size as 2 cm, 3 to 5 cm, and more than 5 cm, and the number of positive nodes as 0, 1 to 3, and 4. For primary therapy, we classified patients as having received a mastectomy, breast conserving surgery followed by radiation therapy, or breast conserving surgery alone. At the baseline and first follow-up interviews, we asked whether patients had received chemotherapy.

Tamoxifen side effects. We assessed potential side effects of tamoxifen using a subset of items developed for the National Surgical Adjuvant Breast and Bowel Project Breast Cancer Prevention Trial¹³ that included fatigue; weight loss and gain; hot flashes; nausea; increased and decreased appetite; vaginal discharge, bleeding or spotting, and dryness; breast sensitivity or tenderness; fluid retention; and depression. We conservatively considered only the number of severe symptoms reported and classified the number of reported severe side effects as 0, 1, or 2.

Quality of life. We measured physical function using the Medical Outcomes Study Short Form–36 10-item Physical Function Index (PFI-10), and mental health, using the Medical Outcomes Study five-item Mental Health Index (MHI-5).¹⁴ The responses for both of these instruments were scaled from 0 to 100, with higher scores reflecting better physical function or better mental health. We used the psychosocial subscale of the Cancer Rehabilitation Evaluation System–Short Form (CARES-SF)¹⁵ to capture cancer-specific aspects of quality of life. This 17-item scale assesses cancer-related anxiety, discomfort with body changes, difficulty sleeping, difficulty concentrating, communication with friends and relatives, and worry about whether the cancer is progressing or recurring, among others. Item scores range from 1 to 4 (higher score indicating more problems), and scores were transformed to a 0- to 100-point scale, with 100 being the most favorable score.

Medical interaction. We determined whether the patient had been referred to a medical oncologist or not, and we used the four-item medical interaction subscale of the CARES-SF to assess subjects’ problems communicating with doctors. The overall score was summed as described in the Quality of life subsection for the psychosocial subscale.

Beliefs about risks and benefits of tamoxifen. To measure subjects’ perception of the risks and benefits of tamoxifen, at each interview, we asked a series of 11 questions that addressed both the risks and benefits of tamoxifen. For example, the questions about benefits included: (1) "The likelihood that tamoxifen would reduce the risk of your breast cancer coming back," and (2) "The likelihood that tamoxifen will reduce your risk of heart disease." Questions about risks included: (1) "The risk of tamoxifen causing other serious problems, for example, phlebitis or endometrial cancer," and (2) "Having to make extra doctor visits to have your tamoxifen treatment monitored." For each item, patients selected from among five response options that ranged from "very influential" to "not influential at all," and included "don’t know" in relation to their decision-making about tamoxifen treatment. Based on a factor analysis that confirmed the presence of two distinct scales, we grouped the items into those that measured the benefits (pros) of tamoxifen and those that measured the risks (cons). The pro and con scores were transformed to range from 0 to 100. We subtracted the risks score from the benefits score to create a "decisional balance" variable.

Analytic Methods
We explored the patterns of tamoxifen discontinuance by calculating the overall risk of discontinuance. Because about one-third of the sample did not participate for the full 2 years of follow-up, we also calculated the risk of discontinuance, accounting for those who withdrew from the study. We determined the rate of discontinuance within each interview interval and then calculated the risk based on the within-interval rates.¹⁶

Our interviews did not ask for the dates that women started or stopped tamoxifen. Furthermore, many of our potential predictors were ascertained at each interview. For these reasons, we analyzed our data by comparing each woman who discontinued therapy to five women who started tamoxifen therapy at the same time and were continuing to take tamoxifen at the time when the woman who discontinued had stopped. For the predictors measured at multiple time points (eg, number of medications, tamoxifen adverse effects, PFI-10, MHI-5, CARES-SF subscales, and decisional balance scale) we compared those who had discontinued with those who continued, using data from the interview prior to the interview during which those who had discontinued reported that they had stopped taking tamoxifen.

We categorized our continuous variables, including number of comorbidities, medications, adverse effects, PFI-10, MHI-5, and CARES-SF subscales, because we did not want to assume an exponential relationship between these variables and discontinuance. Because there were limited extant data on which to base decisions about appropriate cut-points, we categorized these variables into quartiles based on the distributions observed in the adherent women. For the decisional balance score, we dichotomized the variable as positive versus neutral or negative scores.

We calculated odds ratios and 95% CIs using conditional logistic regression. We developed our multivariate model beginning with all variables that were predictors of discontinuance at the bivariate level, as well as potential confounders. Variables were considered to be confounders if they changed the estimate of effect by at least 10%. Variables that remained significant predictors of discontinuance in our multivariate models were included in our final model. All analyses were conducted using SAS version 8.2 (SAS Institute, Cary, NC).

	RESULTS

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Of the 690 women who completed a baseline interview for the parent study,¹³ 597 (87%) were ER-positive and potentially eligible for study. Of these, 516 (86%) were prescribed and took tamoxifen, and are the basis of this report. Overall, 88 (17%) of the women who began taking tamoxifen stopped the drug regimen during the 2-year follow-up period. Accounting for losses to follow-up, the prevalence of discontinuance was 21%. Of the women who stopped taking tamoxifen, the majority (n = 60; 68%) took it for less than 1 year. We compared those who took tamoxifen for less than 1 year, with those who took it for more than 1 year but less than 2 years. The groups were similar with respect to sociodemographic, tumor, and treatment characteristics. The early quitters were somewhat less likely to have positive baseline decisional balance scores (67% v 86%; P = .06) than were the later quitters.

Characteristics of the study sample are presented in Table 1. The majority were 70 years or older and were high school graduates. Most had some insurance coverage for medications, and, as a result, monthly out-of-pocket medication costs were generally low. Few perceived their financial resources to be inadequate. One-third had three or more clinically important comorbidities, and more than 40% took four or more prescription medications. Approximately 20% had tumors with high-risk characteristics by virtue of size and node positivity, and almost all received standard primary tumor therapy (either mastectomy or breast conserving surgery followed by radiation therapy).

	DISCUSSION

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Our observed discontinuance rate in this older sample of women is similar to previous estimates from both clinical trials and observational studies of tamoxifen therapy.^4,6,7 In general, rates of tamoxifen adherence are higher than those observed for other medications, including hormone replacement therapy.¹⁶ This may be due to its perceived role in protecting women from the recurrence of a life-threatening disease—namely, breast cancer. This threat may be perceived to be more real and immediate than that, for example, posed by heart disease. This view is supported by the very strong relationship between our decisional balance measure and adherence. In keeping with the prediction of the TTM, adherence was sustained when women perceived that the benefits of therapy outweighed the risks, whereas discontinuance was likely when perceived risks outweighed, or were similar to, benefits.

This finding for decisional balance is consistent with the work of Horne and Weinman,¹⁷ who posited that medication adherence is influenced by individuals’ internal cost-benefit analysis. This concept is very similar to the decision-making model of Janis and Mann that is a key underpinning of the TTM of Behavior Change.¹⁰ Janis and Mann view all human decision making as emanating from a balance sheet of the pros and cons of a given behavior.¹⁸ To test their hypothesis, Horne and Weinman developed a necessity of the prescribed medication, minus concerns about the potential adverse effects of taking it (difference) score. In a cross-sectional study of patients with asthma, renal or cardiac disease, or cancer, they observed that their difference score explained the majority of the observed variance in self-reported adherence, with the relationship being the strongest in the oncology patient group.¹⁷

The strong relationship of our own pro-minus-con score to longer-term adherence and discontinuance suggests that how patients perceive the risks and benefits of tamoxifen therapy is critical for sustaining adherence after the immediate threat of a breast cancer diagnosis has passed and patients have recovered from effects of their primary tumor therapy. Moreover, our data at least preliminarily suggest that our measure may be able to identify those at risk for not taking tamoxifen when prescribed, as well as those at risk for premature discontinuation.

A serious prognostic factor, having four or more positive axillary lymph nodes, was also associated with tamoxifen discontinuance. For these women, for reasons that are not clear, this risk was not integrated into their personal decisional balance. Although the numbers are small, almost half of the women with four or more positive lymph nodes who stopped their tamoixfen did not receive chemotherapy, putting them at particularly high-risk of recurrence. Although we explored a wide range of associations, we do not have a coherent explanation for this finding. Because it is based on very small numbers and the CI is wide, caution in interpretation is warranted, as are additional studies.

To our knowledge, ours is one of the first empirical studies to test the TTM in the setting of breast cancer treatment in older adults, though it has been applied to cancer prevention and early detection behaviors with success.^19,20 As such, the results are encouraging and suggest a role for the model in designing interventions to promote medication adherence, as well as identifying those at high risk of discontinuance. As more oral chemotherapeutic agents are developed and become part of the standard oncologic armamentarium, it will be important to incorporate into clinical practice, strategies that maximize adherence to, and therefore the positive therapeutic effects of, these agents.²¹

Although our study is the largest to date that focuses on tamoxifen adherence in older breast cancer patients, its limitations must be kept in mind. First, this convenience sample of women was mostly white, well-educated, and relatively well-insured. Second, our outcome measure was ascertained by self-report and reflected adherence versus discontinuance only; we did not address the circumstance of intermittent adherence. We also did not consider less than daily taking of tamoxifen as a measure of nonadherence. Third, we did not collect detailed information regarding the reasons for discontinuance, including what proportion was related to serious complications, such as thromboembolic events.

Older women bear a disproportionate burden of breast cancer mortality. In addition to clarifying what constitutes effective primary tumor therapy,²² maximizing the benefit of tamoxifen therapy is an important therapeutic goal. Regular visits for recurrence surveillance, as well as visits to primary care providers, are critical opportunities to inquire about and to promote adherence to tamoxifen.

	Authors’ Disclosures of Potential Conflicts of Interest

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The authors indicated no potential conflicts of interest.

	NOTES

 
Supported by research grant R01 CA/AG70818 from the National Cancer Institute and National Institute on Aging, and R01 CA84506, K05 CA92395, and K07 CA87724 from the National Cancer Institute.

Authors’ disclosures of potential conflicts of interest are found at the end of this article.

	REFERENCES

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION Authors’ Disclosures of... REFERENCES

 
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4. Fisher B, Constantino JP, Redmond C, et al: A randomized clinical trial evaluating tamoxifen in the treatment of patients with node-negative breast cancer who have estrogen-receptor-positive tumors. N Engl J Med 320:479-484, 1989[Abstract]

5. Powles T, Eeles R, Ashley S, et al: Interim analysis of the incidence of breast cancer in the Royal Marsden Hospital tamoxifen randomised chemoprevention trial. Lancet 352:98-101, 1998[Medline]

6. Fisher B, Constantino JP, Wickerham DL, et al: Tamoxifen for prevention of breast cancer: Report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J Natl Cancer Inst 90:1371-1388, 1998[Abstract/Free Full Text]

7. Demissie S, Silliman RA, Lash TL: Adjuvant tamoxifen: Predictors of use, side effects, and discontinuation in older women. J Clin Oncol 19:322-328, 2001[Abstract/Free Full Text]

8. Partridge AH, Wang PS, Winer EP, et al: Nonadherence to adjuvant tamoxifen therapy in women with primary breast cancer. J Clin Oncol 21:602-606, 2003[Abstract/Free Full Text]

9. Vermeire E, Hearnshaw H, Van Royen P: Patient adherence to treatment: Three decades of research—A comprehensive review. J Clin Pharm Ther 26:331-342, 2001[CrossRef][Medline]

10. Prochaska JO, Velicer WF, Rossi JS, et al: Stages of change and decisional balance for 12 problem behaviors. Health Psychol 13:39-46, 1994[CrossRef][Medline]

11. Silliman RA, Guadagnoli W, Rakowski WR, et al: Adjuvant tamoxifen prescription in women 65 years and older with early stage breast cancer. J Clin Oncol 20:2680-2688, 2002[Abstract/Free Full Text]

12. Greenfield S, Apolone G, McNeil BJ, et al: The importance of co-existent disease in the occurrence of postoperative complications and one-year recovery in patients undergoing total hip replacement: Comorbidity and outcomes after hip replacement. Med Care 31:141-154, 1993[CrossRef][Medline]

13. Day R, Ganz PA, Constantino JP, et al: Health-related quality of life and tamoxifen in breast cancer prevention: A report from the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J Clin Oncol 17:2659-2669, 1999[Abstract/Free Full Text]

14. Ware JE: SF-36 Health Survey: Manual and Interpretation Guide. Boston, MA, The Health Institute, 1993

15. Schag CAC, Ganz PA, Heinrich RL: Cancer Rehabilitation Evaluation System–Short Form (CARES-SF): A cancer specific rehabilitation and quality of life instrument. Cancer 68:1406-1413, 1991[CrossRef][Medline]

16. Writing Group for the Women’s Health Initiative: Risks and benefits of estrogen plus progestin in healthy postmenopausal women: Principal results from the Women’s Health Initiative randomized controlled trial. JAMA 288:321-333, 2002[Abstract/Free Full Text]

17. Horne R, Weinman J: Patients’ beliefs about prescribed medicines and their role in adherence to treatment in chronic physical illness. J Psychosom Res 47:555-567, 1999[CrossRef][Medline]

18. Janis IL, Mann L: Decision Making: A Psychological Analysis of Conflict, Choice and Commitment. London, UK, Cassel and Collier Macmillan, 1977

19. Ruggiero L: Transtheoretical model: Applications in the prevention and treatment of cancer. Med Pediatr Oncol 1:69-74, 1998 (suppl 1)

20. Rakowski W, Stoddard AM, Rimer BK, et al: Confirmatory analysis of opinions regarding the pros and cons of mammography. Health Psychol 16:433-441, 1997[CrossRef][Medline]

21. Partridge AH, Avorn J, Wang PS: Adherence to therapy with oral antineoplastic agents. J Natl Cancer Inst 94:652-661, 2002[Abstract/Free Full Text]

22. Silliman RA: What constitutes optimal care for older women with breast cancer? J Clin Oncol 21:3554-3556, 2003[Free Full Text]

Submitted November 12, 2003; accepted May 26, 2004.

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Fink, A. K. Articles by Silliman, R. A. Search for Related Content PubMed PubMed Citation Articles by Fink, A. K. Articles by Silliman, R. A.