Affiliations of authors: M. Stefanek, W. Nelson, Behavioral Research Program, Division of Cancer Control and Population Sciences, National Cancer Institute, Bethesda, MD; L. Hartmann, Division of Medical Oncology, Mayo Clinic, Rochester, MN.
Correspondence to: Michael Stefanek, Ph.D., National Institutes of Health, 6130 Executive Blvd., EPN 4066, Bethesda, MD 20892 (e-mail: ms496r{at}nih.gov).
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ABSTRACT |
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INTRODUCTION |
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"Bilateral prophylactic mastectomy is associated with a reduction in the risk of breast cancer by as much as 90% among women with an increased risk of breast cancer due to a strong family history of breast cancer. Because of the physical and psychological effects of bilateral mastectomy and the irreversibility of the procedure, decisions regarding this option must be carefully considered on an individual basis in association with risk assessment and counseling."
CancerNet, National Cancer Institute (1)
"Although prophylactic mastectomy is never recommended, it may sometimes be envisaged ... The Ad Hoc Committee is strongly opposed to the use of prophylactic mastectomy for women under 30 years of age .... it may be envisaged for women with a lifetime risk of more than 60% of developing breast cancer. ..."
The 1998 French National Ad Hoc Committee (2)
These statements illustrate the controversy surrounding bilateral mastectomy and the clinical dilemma it poses for health-care providers and women at increased risk of developing breast cancer. In the past, bilateral prophylactic mastectomy has been performed on women with a family history of breast cancer, painful breasts, "cancerphobia," or a history of breast biopsies with and without proliferative disease (3). More recently, the availability of BRCA1/2 mutation testing has increased interest in prophylactic surgery. Despite increased interest (4,5), there remains no clear consensus on the indications for this surgery. Part of the controversy may be attributed to the historical lack of data on the effectiveness of the surgery in preventing breast cancer. However, since a review of the issues surrounding bilateral prophylactic mastectomy 5 years ago (3), data now suggest that the surgery may significantly reduce risk, although it may not be completely prophylactic (6). Thus, we advocate labeling this surgery risk-reduction mastectomy (RRM). This term not only is more precise and more consistent with recently published data but also may facilitate understanding among health-care disciplines and between women at risk and their health-care providers.
Although better estimates of the effectiveness of RRM are now available, there continue to be many unresolved issues. These issues limit our understanding of how best to help both women at increased risk of developing breast cancer and their health-care providers make decisions that are based on solid empirical data. We thus review what is known about RRM and delineate areas requiring further study. For this purpose, a literature search of English language, peer-reviewed studies published between 1995 and 2000 was conducted. The search used PubMed®, which provides access to MEDLINE® and other life-science journals, on the search terms "prophylactic mastectomy" and "bilateral prophylactic mastectomy." Abstracts, letters, dissertations, and case studies were excluded. Finally, we excluded articles that did not focus on bilateral prophylactic mastectomy (versus unilateral) or did not focus on our areas of interest as follows: 1) the effectiveness of RRM, 2) the perception of RRM among women at increased risk of breast cancer and health-care providers, 3) the decision-making process for follow-up care of women at increased risk, and 4) satisfaction and psychosocial sequelae of RRM. Twenty-nine references were identified. They were included in this review along with other relevant references.
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EFFECTIVENESS |
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Three data sources inform us to various degrees about the risk-reduction potential of RRM: 1) studies of women who underwent reduction mammoplasty, 2) decision-analysis models, and 3) retrospective data from women who have undergone RRM.
Reduction mammoplasty data are available from two major studies conducted in Denmark (7,8). These data suggest that removing a substantial volume of breast tissue reduces the likelihood of breast cancer development, with the risk of breast cancer reduced by as much as 50%.
Several investigators (9,10) have used decision-analysis methodology to assess survival benefits of RRM among BRCA1/2 mutation carriers. This method involves developing a theoretic model to facilitate clinical decision making. In these studies, a simulated cohort of 30-year-old BRCA1/2 mutation carriers was used to construct a survival model on the basis of cumulative breast cancer incidence rates (11,12) and survival data from the Surveillance, Epidemiology, and End Results1 (SEER) database (13). The models assumed an 85% (9) and a 90% (10) reduction in risk for RRM and used three different risk estimates of breast cancer, ranging from 40% to 85%. RRM demonstrated an increase in life expectancy at all risk levels. In one study (9), survival was increased 2.95.3 years; in the other study (10), survival was increased 2.83.4 years. Gains in life expectancy declined with the age of the woman at the time of surgery. Gains were minimal for women aged 60 years and older (9). These models suggest that RRM confers survival advantages.
Two studies (6,14) have retrospectively tracked incidence and survival data for women after RRM and represent a more direct measure of the value of RRM in reducing risk. The first study (14) included 1500 women who had undergone subcutaneous mastectomy and were followed an average of 9 years after surgery. This dataset was established in the mid-1970s by soliciting patients from members of the American Board of Plastic Surgery. One hundred sixty-five plastic surgeons contributed to this dataset. Six of the 1500 women developed breast cancer. These data were used to support the position that RRM significantly decreased risk. No information was provided about the number of breast cancers that would have been expected in this group or about the degree of risk reduction as a function of surgery. The study had a number of limitations, including the potential for biased selection of patients with a favorable outcome, a 30% loss to follow-up, a lack of defined breast cancer risk, and no central pathology review.
More recently, 639 women with a family history of breast cancer who had undergone RRM between 1960 and 1993 were identified and recontacted (6). Women were classified as high risk (n = 214) or moderate risk (n = 425) by their family history of breast cancer: High-risk women had family histories suggestive of an autosomal-dominant predisposition to breast cancer (Table 1), and women at moderate risk had family histories that did not meet one of the high-risk criteria. Four moderate-risk women and three high-risk women developed breast cancer between 2 and 25 years after RRM.
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PERCEPTIONS OF RRM: HEALTH-CARE PROVIDERS |
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PERCEPTIONS OF RRM: WOMEN AT RISK OF BREAST CANCER |
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The second study (20) that used a vignette format surveyed 426 unaffected women with a family history of breast cancer. In this study, only 5% of the women reported that they would be likely or very likely to undergo RRM if they tested positive for BRCA1/2 mutations. The rate of RRM acceptability in this study was considerably lower than the acceptability rates of the previous studies, and potentially may be accounted for by differences in vignette content, the instructional set, or cultural attitudes and beliefs (26).
Several studies (17,27,28) have examined RRM perception among BRCA1/2 mutation carriers. In an Austrian investigation of 13 unaffected BRCA1/2 carriers, the investigators reported that at 5 months after disclosure of test results, only one (8%) of 13 unaffected carriers certainly would or would be likely to undergo RRM (27). A second study (28) that followed unaffected BRCA1/2 mutation carriers up to 12 months after testing found that only one (3%) of 29 women actually underwent RRM.
In contrast to these findings, a recent investigation from the Rotterdam Family Cancer Clinic (17) found that 76 (55%) of 139 unaffected women with BRCA1/2 mutations chose to undergo RRM. It should be noted that chemoprevention was not offered to these women.
Thus, the data suggest that RRM is a serious consideration for women at increased risk because of a family history of breast cancer. The data provide some support for variables such as breast cancer worry and risk perception being positively correlated with the decision to choose RRM over screening. However, these studies suffer somewhat from differences in assessment strategies. For example, although some studies inquired directly about follow-up preferences, other studies used a vignette format to evaluate preferences. On the other hand, it is hard to draw conclusions about the choices of BRCA1/2 mutation carriers because the few studies that have examined mutation carriers have had small sample sizes. It is difficult to explain why one investigation (17) found a much larger proportion of women selecting surgery than the other studies. These differences might be accounted for by cultural differences, differences in health-services delivery systems, differences in which medical specialties facilitated the discussions of follow-up options, or differences in the type of follow-up information provided (26). For all of these studies, it is unclear what information was provided about the risks and benefits of RRM. This information could have substantially affected how women at high risk viewed RRM. However, the few data that have accumulated are consistent with the view that health-care providers should discuss this option with women at increased risk of breast cancer.
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DECISION MAKING: OPTIONS FOR CLINICAL CARE |
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SURGICAL OPTIONS |
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SCREENING MAMMOGRAPHY |
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Another variable in the mammography screening risk/benefit equation for at-risk women in their forties is screening sensitivity. In one study that evaluated sensitivity of first screening mammography (41), women younger than 50 years old who had a family history of breast cancer had lower mammography sensitivity than women without a family history. It is postulated that the lower mammographic sensitivity observed in young women with a family history of breast cancer may be because of more rapidly growing tumors, which would yield more interval cancers (41,42).
Mammography carries with it a number of potential risks, including the psychological distress that may accompany a false-positive mammogram requiring additional diagnostic evaluation (4345). In one study (44) of 2400 women aged 4069 years who underwent screening mammography over a 10-year period, nearly one fourth of the women experienced at least one false-positive mammogram. If a woman underwent 10 mammographic examinations, her estimated cumulative risk of having a false-positive mammogram was nearly 50%. Other potential risks include a sense of false reassurance resulting from a mammogram that is incorrectly read as normal (46), the theoretical risk of radiation-induced tumors (47,48), and overdiagnosis and treatment of clinically insignificant lesions (46,49,50).
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SCREENING CBE |
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BREAST SELF-EXAMINATION |
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CHEMOPREVENTION |
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The BCPT to date has not evaluated the efficacy of tamoxifen in reducing the risk of breast cancer among BRCA1/2 mutation carriers, although this analysis is under way. Although some believe that this high-risk subgroup might be appropriate for tamoxifen therapy (62), others caution that, because 70%80% of tumors that develop in women with BRCA1 mutations are estrogen receptor negative, tamoxifen may not be as effective (63). There is one report using a casecontrol design in BRCA1/2 mutation carriers that showed a significant reduction in contralateral breast cancers in women who had used adjuvant tamoxifen (64). However, there are several concerns with this study, including lack of information about the estrogen receptor status of the patients. Presumably, women given adjuvant tamoxifen would have been more likely to have estrogen receptor-positive disease, so these results cannot necessarily be generalized to all mutation carriers. Also, there were very wide CIs around the risk-reduction estimates, with an actual increase in contralateral events in women who used tamoxifen for more than 4 years.
Despite much promise as a chemoprevention agent, a number of questions remain about tamoxifen and the conflicting data from two European trials that yielded negative results (65,66). The optimal dose and duration of tamoxifen treatment are not known nor are there sufficient data to determine whether tamoxifen confers an overall health benefit or improved survival (63,67). Because 96% of the participants in the BCPT were white, the generalizability of the BCPT findings to nonwhite women is not known. There are also insufficient data to determine the efficacy of tamoxifen when administered with hormonal agents, because women in the BCPT were not permitted to take hormone-replacement therapy, oral contraceptives, or androgens while in the trial. It is possible, at least theoretically, that hormonal agents might interfere with tamoxifen's effectiveness in reducing breast cancer risk.
Raloxifene, which was approved by the FDA in 1997 for the prevention of osteoporosis in postmenopausal women, is another drug that holds promise as an agent for breast cancer risk reduction. The Study of Tamoxifen and Raloxifene Trial (STAR) for the Prevention of Breast Cancer (61) is a randomized, double-blind study designed to determine whether raloxifene is more or less effective than tamoxifen in reducing the incidence of invasive breast cancer in postmenopausal women. Additionally, the Study of Tamoxifen and Raloxifene Trial will evaluate the toxicity of these regimens and their effect on the quality of life of participants. It is anticipated that 22 000 women will be accrued from more than 400 centers in the United States, Puerto Rico, and Canada.
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DECISION MAKING: PREDICTORS |
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PSYCHOSOCIAL SEQUELAE OF RRM |
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Studies (34,71) examining psychosocial sequelae beyond simply satisfaction with the decision to undergo RRM and other aspects of the surgery have been scarce. One investigation (34) assessed the large sample of women described previously as part of the RRM follow-up study (6). Of the 639 women in this sample, 572 (90%) responded to questionnaires assessing satisfaction with their decision to undergo RRM and their emotional status at a median follow-up of 14.5 years. Seventy percent reported being satisfied or very satisfied with their decision to undergo RRM, with 67% reporting that they definitely or probably would make the same decision again. Thirty-six percent of the variance in satisfaction was explained by the following four factors: 1) satisfaction with appearance, 2) lower levels of stress, 3) fewer problems with implants, and 4) physician's advice to have the surgery. Patients reporting higher levels of satisfaction with their appearance, less stress, and fewer problems with implants after surgery reported higher levels of satisfaction. Patients who reported that their physicians' recommendations were the primary reason for having an RRM reported greater dissatisfaction with the procedure. Seventy-four percent of the respondents reported decreased emotional concern about developing breast cancer. The majority of women reported no change or a favorable change in their levels of emotional stability, stress, self-esteem, sexual relationships, and feelings of femininity.
One prospective study conducted in the U.K. (71) examined psychological morbidity, anxiety, body image, and changes in sexual functioning among 79 high-risk women who elected to undergo RRM and 64 high-risk women who were offered but decided against RRM. Six and 18 months after surgery, among the women who accepted RRM, psychological morbidity and anxiety had decreased significantly; in contrast, among the women who declined the surgery, psychological morbidity and anxiety were not significantly reduced. No significant changes in sexual functioning were reported in either group.
Collectively, these data suggest that women report satisfaction with their decision to have RRM and adjust well emotionally after surgery, although satisfaction with reconstruction may be less than optimal.
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RESEARCH NEEDS |
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NOTES |
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We thank Dr. Kathy Helzlsouer, The Johns Hopkins School of Public Health, Baltimore, MD, for her assistance in reviewing portions of this manuscript and Dr. Barbara Rimer and Dr. Robert Croyle, National Cancer Institute, Bethesda, MD, for their reviews and recommendations.
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Manuscript received January 29, 2001; revised June 22, 2001; accepted July 9, 2001.
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