Special Report
Decision Analysis — Effects of Prophylactic Mastectomy and Oophorectomy on Life Expectancy among Women with BRCA1 or BRCA2 Mutations
N Engl J Med 1997; 336:1465-1471May 15, 1997
- Abstract
Background
Women with BRCA1 or BRCA2 mutations have an increased risk of breast cancer and ovarian cancer. Prophylactic mastectomy and oophorectomy are often considered as ways of reducing these risks, but the effect of the procedures on life expectancy has not been established.
Methods
In a decision analysis, we compared prophylactic mastectomy and prophylactic oophorectomy with no prophylactic surgery among women who carry mutations in the BRCA1 or BRCA2 gene. We used available data about the incidence of cancer, the prognosis for women with cancer, and the efficacy of prophylactic mastectomy and oophorectomy in preventing breast and ovarian cancer to estimate the effects of these interventions on life expectancy among women with different levels of risk of cancer.
Results
We calculated that, on average, 30-year-old women who carry BRCA1 or BRCA2 mutations gain from 2.9 to 5.3 years of life expectancy from prophylactic mastectomy and from 0.3 to 1.7 years of life expectancy from prophylactic oophorectomy, depending on their cumulative risk of cancer. Gains in life expectancy decline with age at the time of prophylactic surgery and are minimal for 60-year-old women. Among 30-year-old women, oophorectomy may be delayed 10 years with little loss of life expectancy.
Conclusions
On the basis of a range of estimates of the incidence of cancer, prognosis, and efficacy of prophylactic surgery, our model suggests that prophylactic mastectomy provides substantial gains in life expectancy and prophylactic oophorectomy more limited gains for young women with BRCA1 or BRCA2 mutations.
Media in This Article
Figure 2
Gains in Life Expectancy among Women with BRCA1 or BRCA2 Mutations, According to the Risk of Breast and Ovarian Cancer.Figure 1
Gains in Life Expectancy among Women with BRCA1 or BRCA2 Mutations, According to Age, Cumulative Risk of Cancer, and Type of Prophylactic Surgery.Article Activity
- Article
Genetic tests are now available for the detection of mutations in the BRCA1 and BRCA2 genes. Among women who carry germ-line mutations in these genes, the cumulative risk of breast cancer is estimated to range from 40 percent to 85 percent, and for ovarian cancer the cumulative risk ranges from 5 percent to 60 percent, depending on the population from which the data were derived.1-5 By comparison, among women in the general U.S. population, the cumulative risk of breast cancer is 12 percent and that of ovarian cancer is 1.5 percent.6 Intensified screening may identify disease at a favorable stage, but it does not prevent cancer.7-9 For this reason, women who carry mutations predisposing them to breast or ovarian cancer may consider prophylactic mastectomy or oophorectomy, or both, despite the lack of data on the long-term outcomes of these procedures. Neither approach completely protects against cancer; cases of breast cancer after bilateral mastectomy and of peritoneal ovarian carcinomatosis after bilateral oophorectomy are well documented.10-12
Even if precise estimates of the efficacy of prophylactic surgery were available, decisions about whether or when to undergo these procedures would be complex. The magnitude of the potential benefit depends on the risk of cancer associated with specific mutations, the prognosis of the tumors in carriers of the mutations, and the extent to which relief of anxiety could result from surgical prophylaxis. These benefits must be weighed against an array of potential costs including surgical complications and the impact of mastectomy or oophorectomy on women's self-image, as well as on their sexual and reproductive function.13,14 The highly personal decision to undergo prophylactic surgery would be facilitated if women and their doctors had clear, tailored data on the effects of prophylactic surgery on medical outcomes.15
To address this clinical dilemma, we developed a decision analysis to provide estimates of the effect of prophylactic surgery on life expectancy among women who carry BRCA1 or BRCA2 mutations. Using available data on the efficacy of the procedures, risk of cancer, and prognosis for various types of tumor, we calculated the gains in life expectancy that were associated with prophylactic surgery, as compared with no prophylactic surgery.
Methods
Model Design
In a Markov model,16,17 we constructed hypothetical cohorts of women, defined according to age and risk of cancer, who were evaluated annually for the development of new breast and ovarian tumors, tumor progression, and death. Breast cancer was classified as local, locally recurrent, or metastatic, and ovarian cancer was classified as local or advanced. Nine strategies that included both immediate prophylactic surgery and prophylaxis after a delay of 10 years were considered: (1) immediate prophylactic mastectomy and oophorectomy, (2) immediate prophylactic mastectomy and delayed oophorectomy, (3) immediate prophylactic oophorectomy and delayed mastectomy, (4) delayed mastectomy and delayed oophorectomy, (5) immediate prophylactic mastectomy only, (6) delayed prophylactic mastectomy only, (7) immediate prophylactic oophorectomy only, (8) delayed prophylactic oophorectomy only, and (9) no prophylactic surgery. We assumed that after prophylactic oophorectomy, women continued to receive hormone-replacement therapy until the age of natural menopause; therefore, prophylactic oophorectomy was assumed to have no effect on the probability of breast cancer.
Data and Assumptions
The probabilities used in our model are listed in Table 1Table 1
Base-Line Probabilities..Incidence of Cancer
Early estimates of the cumulative risk of cancer among carriers of mutant BRCA1 or BRCA2 genes were obtained from families who participated in linkage analysis before the genes were actually identified. Cumulative risks in these families were reported to be as high as 87 percent for breast cancer and 63 percent for ovarian cancer.1 These families were identified because of their striking histories of cancer, which may have introduced a bias favoring the selection of kindreds with high penetrance. Recently, women from families with fewer cases of cancer have undergone genetic testing. It appears that BRCA1 and BRCA2 mutations entail a less extreme risk of cancer for such women.4,5 In a study published in this issue of the Journal, 4 Struewing and colleagues screened a large cohort of Ashkenazi Jews — not selected for a family history of cancer — for the presence of three mutations common in this population. They found a 56 percent cumulative risk of breast cancer and a 16 percent cumulative risk of ovarian cancer associated with these mutations.
Since the specific risks associated with BRCA1 and BRCA2 mutations among the general population are not yet known, we modeled a range of values for the risks associated with BRCA1 and BRCA2 mutations. The lowest level of cumulative risk we considered, 40 percent for breast cancer and 5 percent for ovarian cancer by the age of 70 years (risk level A), represents the lower limit of the 95 percent confidence interval reported by Struewing et al.4 The intermediate level of cumulative risk, 60 percent for breast cancer and 20 percent for ovarian cancer by 70 years of age (risk level B), is similar to the point estimates reported by Struewing et al.4 and Whittemore et al.5 The highest level of cumulative risk we considered, 85 percent for breast cancer and 40 percent for ovarian cancer by the age of 70 (risk level C), reflects the estimated risks in families who were studied by linkage analysis.1 We used the distribution of ages at the diagnosis of cancer up to the age of 70 that was reported by Struewing et al.4 Age-specific rates of incidence beyond the age of 70 were based on data from the Surveillance, Epidemiology, and End Results (SEER) Program.6
Efficacy of Surgical Prophylaxis
There are few studies of the efficacy of prophylactic mastectomy. Reductions as high as 97 percent in the risk of breast cancer have been reported, but the women in these studies did not all have the same indication for surgery, and therefore the initial levels of risk varied. Moreover, they underwent different surgical procedures resulting in variable amounts of residual breast tissue, and follow-up has been short.18,19 After consulting experienced clinicians we chose a conservative estimate of 85 percent for the reduction in the cumulative risk of breast cancer associated with prophylactic mastectomy. Studies of the reduction in the risk of ovarian cancer after prophylactic oophorectomy were performed before gene testing became available, and they have similar limitations.20 On the basis of the one study that evaluated the incidence of cancer among women known to carry BRCA1 mutations by linkage analysis, we assumed a 50 percent reduction in the risk of ovarian cancer after prophylactic oophorectomy.21
Distribution of Tumor Stages
Carriers of BRCA1 or BRCA2 mutations are likely to undergo regular mammography and frequent physical examinations, which could detect breast cancer at an early stage. We therefore assumed that 80 percent of the breast cancers in such women were node-negative, 20 percent were node-positive, and none were metastatic. In contrast, among women at the usual level of risk, 52 percent of cancers are node-negative at diagnosis, 43 percent are node-positive, and 5 percent are metastatic.6 Since there is less evidence that screening for ovarian cancer favorably influences the stage at diagnosis, we assumed, on the basis of data from the SEER Program, that in both carriers of mutations and women at usual risk the likelihood of diagnosing a localized ovarian cancer is 25 percent, and that of finding advanced disease is 75 percent.
Recurrence of Cancer and Mortality
Because the prognostic implications of BRCA1 or BRCA2 mutations in women with breast or ovarian cancer have not been fully characterized, we assumed that the prognosis for carriers with breast cancer was the same, stage for stage, as that for women at usual risk.22-25 The probability of recurrent breast cancer within 10 years of diagnosis was 30 percent for women with node-negative disease and 50 percent for those with node-positive disease.26-28 After 10 years, the annual probability of recurrence was 1 percent. The site of the first recurrence was distant in 75 percent of the cases, and the annual mortality from metastatic breast cancer was 40 percent.29-31 We assumed that carriers of mutations who had ovarian cancer had the more favorable prognosis reported by Rubin et al.32 (44 percent survival at 10 years) and that women at usual risk who had ovarian cancer had the survival rate reported by the SEER Program6,33 (12 percent at 10 years).
Results
Effects of Prophylactic Mastectomy and Oophorectomy on Life Expectancy
The gains in life expectancy resulting from different surgical interventions, as compared with a strategy of no prophylactic surgery, are shown in Table 2Table 2
Age-Specific Gains in Life Expectancy Resulting from Prophylactic Surgery in Women Carrying Mutations of BRCA1 or BRCA2, According to the Level of Cumulative Risk of Cancer by the Age of 70.. For each risk level (A, B, or C), our analysis showed a much greater increase in life expectancy associated with prophylactic mastectomy than with prophylactic oophorectomy. The gain in life expectancy from both prophylactic procedures was greater than the sum of the increases due to each procedure alone, because of the reduction in mortality from the other cancer (breast or ovarian). Gains in life expectancy declined with increasing age because of the decrease in the likelihood of cancer and the decline in the number of years of remaining natural life expectancy. At all three risk levels, 60-year-old women gained less than one year of life expectancy from any prophylactic surgical strategy.Since many women may consider prophylactic surgery only after completing childbearing and lactation, we evaluated several strategies of delayed intervention. At all risk levels, the effect of delaying prophylactic oophorectomy until the age of 40 on the gain in life expectancy was minimal. For example, a 30-year-old woman at risk level B who had prophylactic mastectomy immediately but delayed prophylactic oophorectomy until the age of 40 would gain 5.1 years of life expectancy, as opposed to 5.3 years if she underwent both procedures immediately. The consequences of delaying prophylactic mastectomy until the age of 40 would be greater: 3.6 years as compared with 5.3 years for a woman who underwent mastectomy immediately.
To place the results for carriers of BRCA1 or BRCA2 mutations in perspective, we evaluated the gains in life expectancy for women at usual risk who undergo prophylactic surgery. Figure 1Figure 1
Gains in Life Expectancy among Women with BRCA1 or BRCA2 Mutations, According to Age, Cumulative Risk of Cancer, and Type of Prophylactic Surgery. compares the calculated gains due to prophylactic surgery for 30-year-old women with mutations at risk levels A, B, and C with the increases due to prophylactic surgery for women with usual risk of cancer in the general U.S. population.The incidence of cancer in carriers of mutations is undefined for many mutations in the BRCA1 and BRCA2 genes, but as new information becomes available, our model can be used to approximate the gains in life expectancy associated with prophylactic surgery among women with mutations bestowing any combination of breast- and ovarian-cancer risks (Figure 2Figure 2
Gains in Life Expectancy among Women with BRCA1 or BRCA2 Mutations, According to the Risk of Breast and Ovarian Cancer.). For example, if a specific mutation is found to be associated with a 40 percent cumulative risk of breast cancer and a 30 percent cumulative risk of ovarian cancer, 30-year-old carriers of that mutation might expect to gain an average of four to five years of life expectancy from prophylactic mastectomy and oophorectomy.Sensitivity Analyses
We performed sensitivity analyses to assess the stability of the results of the model when different base-line probabilities and assumptions were used. As shown in Table 2, gains in life expectancy are most sensitive to age and to the risk of cancer associated with mutations of various penetrance levels. Figure 3Figure 3
Results of Sensitivity Analyses. shows the effects of variations in the other influential probabilities for a cohort of 30-year-old women carrying mutations at risk level B. The results are most sensitive to the value used for the efficacy of prophylactic surgery and to the rates of recurrence of breast cancer. If prophylactic mastectomy resulted in nearly complete protection from breast cancer (a 97 percent reduction in risk), it would add 4.8 years of life expectancy. If prophylactic mastectomy were only 25 percent effective, the gain in life expectancy would be just one year. We varied the estimates of the efficacy of prophylactic oophorectomy from 25 percent to 75 percent and found that prophylactic oophorectomy could increase life expectancy by as little as 6 months or as much as 1.5 years.We assumed that women who carry BRCA1 or BRCA2 mutations would be carefully screened and that 80 percent would have breast cancer diagnosed at an early stage. If aggressive screening could identify all breast cancers even sooner, so that the overall 10-year rate of recurrence was 20 percent, the gain in life expectancy due to prophylactic mastectomy in 30-year-old carriers of mutations at risk level B would be 2.5 rather than 4.1 years. Similarly, if enhanced screening could diagnose all ovarian cancers while they were local, prophylactic oophorectomy could prolong life by five months as opposed to one year.
The distribution of ages at the diagnosis of cancer was based on data from Struewing et al., who found a pattern very similar to that derived from linkage analysis.1,4 However, if the actual age at onset is later in some women, our analysis might have overestimated the gains in life expectancy that would result from prophylactic surgery. For example, there is evidence that early-onset breast cancer is relatively rare among women with BRCA2 mutations (see Krainer et al. elsewhere in this issue of the Journal 34). We considered how this might affect our results in a sensitivity analysis. Shifting the age-specific cumulative-risk curves for both breast and ovarian cancer to the right by 10 years results in a gain of 3.7 rather than 5.3 years of life expectancy for 30-year-old women at risk level B who undergo prophylactic mastectomy and prophylactic oophorectomy.
The results of the model are insensitive to changes in other variables. When the values used for the probability of dying as a result of prophylactic surgery, having an incidental tumor detected at the time of surgery, having a local recurrence, and presenting with metastases and the annual probability of dying of advanced breast cancer or ovarian cancer were varied over broad ranges, the gains in life expectancy changed by less than six months.
Discussion
Women found to have BRCA1 or BRCA2 mutations face difficult decisions about ways of reducing their risk of breast or ovarian cancer. Moreover, data concerning the efficacy of the available strategies are limited. Until better methods of cancer prevention are developed, women and their physicians are likely to continue to consider the possibility and timing of prophylactic mastectomy and oophorectomy. It is precisely for these kinds of choices, which must be made under conditions of uncertainty, that decision analysis can be most helpful.
We calculated the effect of prophylactic surgery on survival for women who carry BRCA1 or BRCA2 mutations associated with different levels of risk and found that even when we used conservative estimates for the efficacy of the surgical procedure, the gain in life expectancy resulting from prophylactic mastectomy and oophorectomy was substantial among younger women. Most of the benefit derived from prophylactic mastectomy. In our analysis, prophylactic oophorectomy resulted in, at most, small gains in life expectancy, and postponing oophorectomy until the completion of childbearing reduces its benefit minimally. Because breast cancer is a common disease, our model predicts that even 30-year-old women with the usual level of risk gain some additional life expectancy (eight months) from prophylactic mastectomy and oophorectomy. Prophylactic surgery is obviously unreasonable for these women, but this result helps to anchor the gains in life expectancy for women with BRCA1 or BRCA2 mutations. Decisions about prophylactic surgery must take into account individual preferences about the trade-offs between the loss of breasts and ovaries and the possible relief of anxiety and prolongation of life. Our analysis offers a framework for these personal decisions by furnishing estimates of the medical effect of prophylactic surgery.
Although much has been learned about the penetrance of mutations in certain populations, we are currently unable to predict with any precision the risk of cancer for individual women who have BRCA1 or BRCA2 mutations.35,36 The portion of the range of cumulative risks most applicable to a woman with a BRCA1 or BRCA2 mutation depends on several factors. The gains in life expectancy calculated for women at risk level A may provide guidance about the effect of prophylactic surgery among women with a family history that suggests relatively low penetrance. The gains in life expectancy for women at risk level B may be more applicable to carriers of mutations seen in clinics assessing the risk of cancer, most of whom have several first-degree relatives with breast or ovarian cancer or both (see Couch et al. elsewhere in this issue of the Journal 37). The results for women at risk level C are likely to be relevant only for gene carriers who are members of kindreds with particularly strong histories of early-onset breast cancer or breast and ovarian cancer.
To place our results in context, we compared them with the gains in life expectancy reported in decision analyses for interventions used in patients with other medical conditions (Table 3Table 3
Gains in Life Expectancy Associated with Prophylactic Surgery as Compared with Measures to Prevent Coronary Artery Disease and Treatment of Breast Cancer in 35-Year-Old Women.). The magnitude of the estimated gains in life expectancy for 35-year-old women carrying mutations at risk level B who undergo both prophylactic mastectomy and prophylactic oophorectomy is in the same range as the benefits expected for 35-year-old women who have extraordinarily high cholesterol levels and reduce them to normal.38 The gains from prophylactic surgery for carriers of BRCA1 or BRCA2 mutations may exceed those anticipated from other common strategies to reduce the risk of coronary artery disease and from adjuvant chemotherapy for breast cancer39,40 (and Hillner BE: personal communication).Several limitations in our analysis should be noted. We evaluated only surgical prevention; the effects of hormonal therapies, such as tamoxifen or oral contraceptives, alone or in combination with surgical prophylaxis, were not examined.41 As results from chemopreventive trials become available, our analysis should be expanded to incorporate hybrid medical and surgical strategies. In addition, without long-term, comprehensive data on outcomes, we cannot be sure that prophylactic surgery does not induce adverse effects on life expectancy. Our analysis assumes that premenopausal women who undergo prophylactic oophorectomy receive hormone-replacement therapy until the age at which they would otherwise have undergone natural menopause. However, without hormone replacement, higher rates of mortality due to cardiovascular disease or lower rates of mortality due to breast cancer 42 might alter life expectancy.
Calculated gains in life expectancy should be interpreted carefully. An increase of four years in life expectancy does not imply that an individual woman can anticipate an extra four years of life. Rather, these gains reflect the average benefits for a cohort of women at a defined age and level of risk. A woman with a BRCA1 mutation who undergoes a prophylactic mastectomy but in whom breast cancer was not destined to develop would not gain from the procedure. In contrast, a woman who would have been found to have breast cancer at the age of 40 had she not chosen to undergo a prophylactic mastectomy could benefit considerably.
Individual attitudes toward genetic testing and prophylactic surgery are unpredictable and diverse. Sisters who have identical risks of cancer and similar first-hand experience with how cancer affected their mother may have very different views about these procedures. It is therefore important to find ways of communicating the risks and benefits of preventive strategies that encourage patients to incorporate their personal preferences into their choice of treatment. By providing estimates that create a starting point for making these difficult decisions, the results of our model offer a framework that may help women who carry these gene mutations choose the preventive strategy that is best for them.
Dr. Schrag is the recipient of an Agency for Health Care Policy and Research Health Services Fellowship.
We are indebted to Drs. Milton Weinstein, Carolyn Kaelin, and Michael Muto for their contributions.
Source Information
From the Center for Outcomes and Policy Research (D.S., J.C.W.) and the Division of Cancer Epidemiology and Control (J.E.G.), Dana–Farber Cancer Institute and Harvard Medical School; and the Section for Clinical Epidemiology, Brigham and Women's Hospital and Harvard Medical School (K.M.K.) — all in Boston.
Address reprint requests to Dr. Weeks at the Center for Outcomes and Policy Research, Dana–Farber Cancer Institute, 44 Binney St., Boston, MA 02115.
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