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Patient Reluctance Toward Tamoxifen Use for Breast Cancer Primary Prevention

From the Breast Service, Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: Elisa Rush Port, MD, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, MRI-1026, New York, NY 10021; Fax: 212-794-5812.

	ABSTRACT

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Background: The National Surgical Adjuvant Breast and Bowel Project (NSABP) P-1 trial demonstrated that tamoxifen reduces the incidence of new breast cancers by 49% in women at increased risk for breast cancer development. Tamoxifen does have side effects, however, including marginally increased risks of endometrial cancer and thromboembolic events. In this study, women at increased risk for breast cancer development were offered tamoxifen. Their knowledge of tamoxifen as a chemopreventive agent was assessed, and factors influencing their acceptance of tamoxifen and willingness to take it were determined.

Methods: Forty-three patients were identified who qualified to take tamoxifen for primary prevention. Patients qualified by having at least a 1.7% 5-year risk of developing breast cancer, the criteria for entry into the NSABP P-1 trial. Patients initially completed questionnaires designed to assess their knowledge of tamoxifen and its associated risks and benefits. Patients were then provided neutral educational sessions and literature delineating the actual risks and benefits of tamoxifen. Subsequently, patients’ decisions regarding taking tamoxifen were reassessed.

Results: Mean patient age was 52.8 years, with a range of 39 to 74 years. Ten patients (23.2%) qualified based on the presence of lobular carcinoma in situ (LCIS), seven patients (16.3%) qualified based on increased risk secondary to age >60 years, and 26 patients (60.5%) age range 35 to 59 qualified based on risk profiles demonstrating significantly increased risk. Of the total 43 patients, two (4.7%) elected to start taking tamoxifen. Fifteen patients (34.8%) declined immediately, and 26 patients (60.5%) were undecided initially but ultimately declined. Educational sessions did not influence patients’ decisions. Fear of side effects, including endometrial cancer, thromboembolic events, and menopausal symptoms, was the most commonly cited reason for declining to take tamoxifen.

Conclusions: In this study, the vast majority of patients at increased risk for breast cancer perceived that the risks of taking tamoxifen outweighed the benefits and declined to take it.

Key Words: Tamoxifen • Breast cancer • Chemoprevention • Patient reluctance

	INTRODUCTION

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Breast carcinoma is the most common solid malignancy affecting women in the United States. It is estimated that nearly 200,000 new cases of breast cancer were diagnosed in the year 2000.¹ However, not all women are at equal risk for the development of breast cancer. Specific risk factors that place a woman at substantially increased risk for the development of the disease have been identified. These risk factors include a strong family history of breast cancer, a history of abnormal pathology such as lobular carcinoma in situ (LCIS), or atypical hyperplasia on previous biopsy.²

In 1977, the Food and Drug Administration (FDA) approved the use of tamoxifen for breast cancer treatment after it was shown to decrease the risk of recurrence, improve overall survival, and reduce the incidence of contralateral breast cancers.³ Although tamoxifen was much less effective in reducing recurrence and mortality in women with estrogen-receptor (ER)-negative tumors than in those with ER-positive tumors, it was equally effective in both groups in reducing the development of contralateral cancers. The proportional reduction in contralateral breast cancer in women with either ER-positive or ER-negative tumors was approximately 30%.³

The National Surgical Adjuvant Breast and Bowel Project (NSABP) P-1 trial was initiated in 1992, with the primary aim of evaluating the effectiveness of tamoxifen in preventing breast cancer in women at increased risk. Secondary aims of this trial included evaluating the effects of tamoxifen on the incidence of cardiac events, osteoporotic fractures, and breast cancer-related mortality. Patients were enrolled in the study based on criteria related to increased risk. Patients with a history of LCIS on previous biopsy were eligible based on this risk factor alone. Patients 60 years of age or older also qualified. Patients aged 35 to 59 years who, because of other risk factors, reached the risk threshold of a 60-year-old (1.67% over 5 years) were also eligible. Individual risk for these patients was determined using the Gail model.⁴ This model incorporates patient data on race, age, age at menarche, age at first live birth, number of previous breast biopsies, number of first-degree relatives with breast cancer, and a history of atypical hyperplasia. Each patient’s risk level for developing breast cancer over the ensuing 5 years and over her lifetime was then estimated using this model.

The P-1 trial randomized 13,388 patients to either tamoxifen or placebo and followed them for a mean of 54.6 months. Breast cancer risk was found to be effectively reduced by tamoxifen for patients in all age groups and at all levels of risk. Reductions in breast cancer incidence were most significant for those patients with a history of atypical hyperplasia or LCIS. Thus, in 1998, approximately 20 years after its original approval by the FDA for use in adjuvant treatment of breast cancer, tamoxifen was approved for breast cancer primary prevention.

Tamoxifen does have associated side effects, including increased risks of endometrial cancer and thromboembolic events, an increased risk of requiring surgery for cataract disease, and exacerbation of menopausal symptoms such as hot flashes and vaginal discharge.^5–7 Given these known benefits and risks, a prospective study was undertaken to determine patient interest in and acceptance of electively taking tamoxifen for the purpose of primary prevention.

	MATERIALS AND METHODS

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Patients were identified through the practices of four attending surgeons at Memorial Sloan-Kettering Cancer Center and through the institution’s Special Surveillance Breast Program, which is aimed at the identification and follow-up of women at increased risk for breast cancer. The risk criteria for inclusion in the study were the same as those used for inclusion in the P-1 trial. Exclusion criteria included any one or more of the following: previous tamoxifen use, previous counseling on the risks and benefits associated with taking tamoxifen, a diagnosis of breast cancer, a history of endometrial cancer, or a previous thromboembolic event.

Tamoxifen was offered to those patients at increased risk for breast cancer, and factors influencing their decisions to take or refuse it were assessed. Patients first completed questionnaires designed to assess their knowledge of tamoxifen and its associated risk factors, as well as their attitude toward taking tamoxifen as a preventive agent. Patients were then provided educational sessions and literature delineating the actual risks and benefits of tamoxifen use. Patients’ decisions regarding taking tamoxifen were assessed immediately following these sessions and subsequently reassessed by telephone interview.

	RESULTS

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Forty-three patients were identified who were eligible to take tamoxifen for primary prevention based on the aforementioned criteria. Patient profile data can be found in Table 1. Mean patient age was 52.8 years, with a range from 39 to 74 years. The majority of patients were Caucasian and married. Thirty-four patients (79%) reported having a college or graduate degree.

Of the 43 patients offered tamoxifen, 2 (4.7%) elected to take it. Fifteen patients (34.8%) declined definitively, and 26 patients (60.5%) initially reported being undecided. Neither educational sessions nor distributed literature influenced patient decision-making regarding taking tamoxifen. None of the patients who were initially undecided subsequently elected to take tamoxifen, and none of those who declined tamoxifen immediately changed her decision subsequently. Thus, the total number of patients who ultimately declined to take tamoxifen was 41 (95.3%).

Data regarding patients’ attitudes toward tamoxifen use for primary prevention can be found in Table 2. Of the 41 patients who chose not to initiate tamoxifen chemoprevention, fear of side effects was the most commonly cited reason. The most feared side effects were endometrial cancer and thromboembolic events. Other reasons cited for not wanting to take tamoxifen included a perceived lack of adequate available information on tamoxifen and reluctance to discontinue hormone replacement therapy (HRT). Fifteen of 41 patients (36.6%) cited two or more side effects as the reason for their declining to take tamoxifen.

Two patients elected to take tamoxifen. One of these patients had LCIS and one had atypical hyperplasia. One patient had previously undergone two biopsies; the other had undergone five. Among patients declining to take tamoxifen, the mean number of biopsies per patient was 1.3.

Of the two patients who elected to take tamoxifen, one reported experiencing frequent anxiety (more than once a week) related to developing breast cancer, while the other reported only rarely worrying about breast cancer. In contrast, of those who declined tamoxifen, only 9% reported experiencing breast cancer-related anxiety more than once a week. One of the two patients who elected to take tamoxifen had a higher perceived lifetime risk of developing breast cancer than patients who declined tamoxifen. This patient indicated a perceived 70% chance of developing breast cancer in her lifetime. The other patient who elected to take tamoxifen perceived her lifetime risk to be 25%. In contrast, among patients who declined to take tamoxifen, the mean perceived lifetime risk of developing breast cancer was 35%.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Tamoxifen is currently the only medication approved for breast cancer primary prevention, and for women at increased risk for breast cancer development, it is the only primary prevention alternative to prophylactic surgery. Fear of developing breast cancer and the tendency to overestimate risk are commonplace among women at increased risk for breast cancer development. These facts suggest that an available, proven chemopreventive agent would be widely used. Our data support some elevation of the perceived risk of breast cancer among patients at high risk: while the mean actual risk for this group was calculated at 19%, the mean perceived risk was 40%. Despite this, however, the vast majority of women in our study population declined tamoxifen therapy.

Patient reluctance to take tamoxifen was documented in the three major trials of tamoxifen as a chemopreventive agent. Each of these trials demonstrated a significant rate of attrition,^5,8,9 which was, in part, attributable to patient reluctance to take tamoxifen. In the Italian trial, which randomized 5408 hysterectomized women between the ages of 35 and 70 to receive either tamoxifen or placebo, accrual was terminated early, in part because the patient attrition rate was 26.3%.⁸ The most commonly cited reasons for withdrawal in the Italian trial were side effects and fear of the medication. Similar findings were reported in the Royal Marsden trial, ⁹ in which 2494 women between the ages of 30 and 70 with a family history of breast cancer were randomized to receive either tamoxifen or placebo. Of note, this trial allowed women on HRT to continue therapy, thereby eliminating one common reason given by patients for declining tamoxifen. Despite the fact that 41% of women in this study were on HRT for menopausal symptoms, a significant rate of attrition remained. Lastly, in the P-1 trial, a total of 21.6% of participants (19.7% in the placebo group and 23.7% in the tamoxifen group) discontinued therapy.⁵ The results from these studies, particularly those of the Italian and Royal Marsden trials, suggest that fear of side effects related to tamoxifen may be an obstacle to its achieving widespread use for chemoprevention.

Fear of side effects was the reason most frequently given by the women in our study population for declining tamoxifen therapy. In addition, the majority of women overestimated their risk of developing side effects. In an attempt to counter the effects of any potential bias generated by the physician while presenting patients with the option to take tamoxifen, we involved four physicians in this study. Even after a balanced presentation of the risks and benefits of tamoxifen use for chemoprevention, there was no increase in patient acceptance. The fact that all of the patients who were initially undecided regarding taking tamoxifen ultimately declined to take it raises the possibility that physician presentations were actually negative rather than neutral. Negatively biased physician presentations would certainly affect the outcome of patient decision-making. In addition to the involvement of four different physicians, literature in which the risks and benefits of tamoxifen use were delineated in numerical form was distributed in an attempt to ensure neutrality of presentation.

Many of the patients in our study who declined tamoxifen indicated in discussion that they feared multiple side effects. According to these women, eliminating one side effect, or allaying their fear of one side effect, would have been insufficient to change their decision. In addition, as previously described, there was a substantial discrepancy between the actual risk of developing side effects and the patients’ exaggerated perceived risk. This discrepancy suggests that influences other than the material presented were operative in their decisions to decline tamoxifen. Information was provided to the patients in our study through consultation as well as medical literature. It has been shown in other disease types,¹⁰ however, that patients commonly obtain additional information and input from both medical and nonmedical sources, including family and friends, the Internet, the lay press, as well as other medical professionals. Thus a patient’s fear of side effects may reflect anecdotal experience related to her by women who have taken the medication or by outside information. These outside influences may play a more significant role in patient decision-making than either a neutral presentation by a doctor or data from medical literature, and a questionnaire or discussion may not be able to fully assess their contribution.

In addition to the possibility of outside influences overwhelming objective data presented to the patient, it is possible that healthy patients simply do not wish to take medication on a regular basis. This is often the case, even in patients with known medical ailments. Studies of patient compliance with medication regimens for various diseases, including hypertension, asthma, and diabetes, show high degrees of patient noncompliance despite their knowledge of the potential benefits of these medications.^10,11

One recent study of hypertensive patients indicated that approximately one-third of the patients always take their medication, one-third occasionally take it, and one-third never take it. In addition, approximately 50% of the patients stop taking newly prescribed medication within 6 months.¹¹ Although in this study fear of side effects was frequently cited by these patients as a major reason for discontinuing medication, the authors point out that most antihypertensive agents are not associated with prominent side effects and are well tolerated. Similarly, reluctance to take medication has been demonstrated among asthma patients who are prescribed medications for long-term preventive treatment. In this case, patient reluctance was shown to be connected to a general resistance to taking medication rather than to a fear of associated side effects;¹⁰ asthma patients have been shown to be more inclined to take medication sporadically, restarting therapy when symptoms worsen and discontinuing it when symptoms subside.

Patient noncompliance with medication regimens and reluctance to take medication in general are significant problems in disease states. Extrapolating from these data, it is understandable and highly probable that patients who feel well and are otherwise healthy may be reluctant to take a medication such as tamoxifen for purely preventative purposes, as was the case in our study. It is possible, however, that patients at considerably higher risk for breast cancer, such as BRCA heterozygotes, would be more receptive to tamoxifen therapy. Grann et al.¹² analyzed the effectiveness and impact on quality of life of various risk-reducing strategies for BRCA heterozygotes. Chemoprevention with either tamoxifen, raloxifene, or oral contraceptives; prophylactic surgery; or surveillance were compared for potential overall survival benefit and for impact on patient quality of life. Results suggested that tamoxifen would provide an overall survival benefit in BRCA heterozygotes when compared with surveillance. While prophylactic surgery provided a longer survival benefit than chemoprevention with either tamoxifen or raloxifene, quality-adjusted survival was estimated to be better with chemoprevention than after prophylactic surgery.

One caveat to the conclusions of the study by Grann et al.¹² is the finding that, in contrast to sporadic cancers, most BRCA-associated cancers are ER-negative.¹³ While tamoxifen has been shown to be most effective in reducing the incidence of ER-positive tumors, recent data support tamoxifen’s effectiveness in reducing the risk of new cancers in BRCA heterozygotes.¹⁴ DNA analysis of P-1 participants for BRCA mutations is currently under way. The results of this analysis will provide further information regarding the effectiveness of tamoxifen in BRCA heterozygotes.

Studies have also demonstrated that patient acceptance of and compliance with medication regimens is strongly influenced by the doctor-patient relationship and, specifically, by the quality of their interaction.^10,15,16 In disease states, patients are more likely to comply with medication regimens when they are motivated by their physicians to do so and when they receive a clear message regarding the importance of compliance. The low acceptance rate of tamoxifen by patients from all four practices in this study underscores the fact that a neutral presentation from a physician will most likely not lead to acceptance of a medication such as tamoxifen. Although our study only addressed patients’ initial reactions to taking tamoxifen for chemoprevention, it is likely that the patient-physician interaction will play an important role in maintaining patients on tamoxifen therapy should they choose to initiate it.

The development of new chemopreventive agents for many different tumor types, including breast carcinoma, is an area of active interest and expanding research efforts. The engineering and study of other selective estrogen-receptor modulators (SERMs), such as raloxifene, may result in the availability of alternative chemopreventive agents for patients at increased risk for breast cancer development. Results from the Multiple Outcomes of Raloxifene Evaluation (MORE) trial¹⁷ have indicated that raloxifene, a drug approved for the treatment of osteoporosis, may reduce breast cancer risk. Because of the benefit of raloxifene for treatment of osteoporosis and its lack of endometrial cancer risk, it may provide patients with a more appealing option for breast cancer risk reduction. The NSABP is currently accruing patients to the Study of Tamoxifen and Raloxifene (STAR). This trial may answer some of the many questions that exist about the relative merits of raloxifene as a chemopreventive agent.

Our data indicate significant patient reluctance to taking tamoxifen for breast cancer risk reduction, despite these patients’ increased risk profiles. Clearly, multiple factors contribute to shaping patients’ attitudes toward medication in general and toward tamoxifen specifically. Given this reluctance, a completely neutral approach to the presentation of tamoxifen is unlikely to yield a large number of women taking the medication. While a strong stance in favor of tamoxifen use for breast cancer prevention would most likely result in increased patient acceptance, the appropriateness of strongly promoting a medication with significant side effects for purely preventive purposes remains in question. In the future, further characterization of tamoxifen’s long-term benefits, as well as the introduction of other chemopreventive agents, may lead to a wider acceptance of chemoprevention in general.

	Acknowledgments

 
The authors thank K. Alexandra MacDonald for her editorial contribution in the preparation of this manuscript.

	Footnotes

 
Presented at 53rd Annual Meeting of the Society of Surgical Oncology, New Orleans, Louisiana, March 16–19, 2000.

Received for publication January 18, 2001. Accepted for publication April 4, 2001.

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Port, E. R. Articles by Borgen, P. I. Search for Related Content PubMed PubMed Citation Articles by Port, E. R. Articles by Borgen, P. I. Related Collections Chemotherapy