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Efficacy of Contralateral Prophylactic Mastectomy in Women With a Personal and Family History of Breast Cancer

From the Divisions of Medical Oncology, Biostatistics, Plastic and Reconstructive Surgery, and Clinical Epidemiology, and Departments of Surgery and Laboratory Medicine and Pathology, Mayo Clinic Cancer Center, Mayo Clinic and Mayo Foundation, Rochester, MN; and Department of Pathology, St Vincent’s Hospital, Dublin, Ireland.

Address reprint requests to Lynn C. Hartmann, MD, Division of Medical Oncology, Mayo Clinic, Rochester, MN 55905; email: hartmann.lynn{at}mayo.edu

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To estimate the efficacy of contralateral prophylactic mastectomy in women with a personal and family history of breast cancer.

PATIENTS AND METHODS: We followed the course of 745 women with a first breast cancer and a family history of breast and/or ovarian cancer who underwent contralateral prophylactic mastectomy at the Mayo Clinic between 1960 and 1993. Family history information and cancer follow-up information were obtained from the medical record, a study-specific questionnaire, and telephone follow-up. Life-tables for contralateral breast cancers, which consider age at first breast cancer, current age, and type of family history, were used to calculate the number of breast cancers expected in our cohort had they not had a prophylactic mastectomy.

RESULTS: Of the 745 women in our cohort, 388 were premenopausal (age < 50 years) and 357 were post- menopausal. Eight women developed a contralateral breast cancer. Six events were observed among the premenopausal women, compared with 106.2 predicted, resulting in a risk reduction of 94.4% (95% confidence interval [CI], 87.7% to 97.9%). For the 357 postmenopausal women, 50.3 contralateral breast cancers were predicted, whereas only two were observed, representing a 96.0% risk reduction (95% CI, 85.6% to 99.5%).

CONCLUSION: The incidence of contralateral breast cancer seems to be reduced significantly after contralateral prophylactic mastectomy in women with a personal and family history of breast cancer.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
FOR WOMEN WITH A personal history of breast cancer, the risk of a contralateral event is significantly higher in those who have a family history of the disease. In an early study of contralateral breast cancer risk in women with a family history, Harris et al¹ described a 35% risk of contralateral breast cancer by 16 years after the first breast cancer diagnosis. In contrast, in women without a family history of breast cancer who have had a first event, the risk of a contralateral breast cancer is less than 1% per year.² Obedian et al³ documented a contralateral breast cancer risk of 10% at 15 years in a long-term follow-up study of early-stage breast cancer patients unselected for family history. In women identified to be carriers of mutations in BRCA1 or BRCA2, the contralateral breast cancer risk is considerably higher, ranging from a low of 12% at 5 years in BRCA2 carriers in a Dutch series⁴ to 20% to 31% at 5 years in a group of BRCA1 carriers⁵ and Ashkenazi BRCA1 or BRCA2 carriers.⁶

Thus women with a family history of breast cancer who present with a first breast cancer face several competing risks, including recurrence of their first breast cancer and a contralateral new primary. For some women, therapeutic mastectomy on the affected side and a contralateral prophylactic mastectomy represent the preferred strategy. To our knowledge, there have been no published data regarding the degree of contralateral breast cancer risk reduction achieved with a prophylactic procedure in this setting. In the present study, we followed the course of a group of women with a first breast cancer and a family history of breast cancer and/or ovarian cancer who had a contralateral prophylactic mastectomy (after a therapeutic mastectomy) at the Mayo Clinic between 1960 and 1993. We report the occurrence of second breast cancers in this group and evaluate the frequency relative to the expected occurrence had a prophylactic procedure not been performed.

	PATIENTS AND METHODS

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Identification of Cohort
To identify all women who had a contralateral prophylactic mastectomy performed at the Mayo Clinic, we obtained from our Surgical Index Recording System all individuals who had a unilateral therapeutic mastectomy (either radical or modified radical) and a contralateral subcutaneous mastectomy or total mastectomy (either procedure performed with prophylactic intent) between January 1, 1960, and December 31, 1993. Family history information and cancer follow-up information were obtained from the medical record. A study-specific questionnaire, requesting data on risk factors and cancer occurrences, was sent to all women or, if they were deceased, to their next of kin. When needed to clarify cancer occurrences or family history data, telephone follow-up was also used. A total of 1,643 women were identified; 792 had a family history of breast and/or ovarian cancer.

To calculate the number of contralateral breast cancers expected in this family-history–positive group, we used the Anderson model.^7,8 The Anderson model (see Statistical Analysis) considers only breast cancer events in the family and requires one of three types of pedigrees: parent-affected, sibling-affected, or second-degree relative–affected. Seven hundred forty-two women with a positive family history fit one of the Anderson model categories. Three additional women for whom family history was less clear yet who later developed a contralateral breast cancer were also included in the Anderson model calculations so that our estimated risk reductions would be conservative. Two of these women had uncertain family histories. Although their medical records did not indicate a family history, we were unable to confirm this by questionnaire or telephone. Because the possibility exists that these two women could have a family history of breast cancer that was never documented in the medical record, they were included in the Anderson model calculations by classifying them as if they had second-degree relatives affected; if a first-degree relative had been affected, then we assumed that it would have been recorded in the medical record. The third woman had an affected third-degree relative. She, too, was included in the analysis by classifying her as having an affected second-degree relative. Including these three women because they developed a contralateral breast cancer biases the observed number of second primaries upwards, yielding a more conservative estimate of the risk reduction offered by prophylactic surgery. Thus our final cohort for this analysis included 745 women.

Forty-nine additional women had a positive family history but were not included in the Anderson model calculations. Thirty-one of these women had ovarian cancer in their family but no reported breast cancer. The other 18 women reported third-degree relatives affected with breast cancer. None of these 49 women have developed a post–prophylactic mastectomy breast cancer.

Data Collection and Follow-Up
The study-specific questionnaire solicited information about occurrences of cancer in the proband; surgical morbidities after mastectomy; breast cancer risk factors, including family history; reasons for selecting prophylactic mastectomy; effects on various measures of psychologic and social function; and long-term satisfaction with the procedure.

Prophylactic Surgical Techniques
The technique of subcutaneous mastectomy has been described in detail elsewhere.^9,10 The majority of breast tissue ( 90%) is removed with residual tissue remaining immediately beneath the nipple-areolar complex. The technique of total mastectomy has been described in detail elsewhere.¹¹ With this approach, the entire breast is removed, including the nipple-areolar complex. No axillary node dissection is performed. The pectoralis muscles are preserved.

Pathology Review
All available specimens obtained at therapeutic and prophylactic mastectomy, and in subsequent cases of breast cancer, were reviewed by one of the two participating pathologists. The tissue obtained at prophylactic mastectomy was categorized as follows: normal with nonproliferative changes, proliferative change without atypia, atypia, carcinoma-in-situ, or invasive cancer.

Definition of Post–Prophylactic Mastectomy Breast Cancer
We considered an adenocarcinoma developing on the chest wall or in the axilla on the side of the prophylactic mastectomy to be a post–prophylactic mastectomy breast cancer. Ipsilateral recurrences were not considered to be post–prophylactic mastectomy breast cancer events.

Statistical Analysis
The goal of this study was to compare the observed number of contralateral breast cancer events among our cohort of women who elected contralateral prophylactic mastectomy with that which would be expected had this surgical procedure not been performed. Because family history of breast cancer and menopausal status are two factors that may have a strong influence on the risk of a contralateral event, it is necessary to account for this information in our analyses. To do so, the results reported by Anderson et al^7,8 (which we shall refer to as the Anderson model) were used. The Anderson model was based on 556 women diagnosed with breast cancer who had a medical record indicating that a female relative also had breast cancer. Patients were identified at the M.D. Anderson Cancer Center starting in 1944, with results published in 1985. The Anderson model reported cumulative probabilities of a second primary breast cancer developing in patients classified by pedigree type (mother, sister, or second-degree relative with breast cancer) and menopausal status. The probabilities were reported for single-year intervals up to 10 postoperative years and for 5-year intervals from 10 to 19 postoperative years. These cumulative probabilities were used to compute hazard rates per person-year for each year of follow-up. Hazard rates were assumed constant within each of the reported 5-year intervals. The Anderson model can be used to predict a woman’s risk only until 19 years after her breast cancer. For our study participants who were followed-up beyond 19 years, the hazard rate at 19 years was applied to each subsequent year of follow-up. Hazard rates were applied to the observed person-years of follow-up to obtain expected numbers of contralateral breast cancers. The observed person-years began at the time of prophylactic surgery and ended at the time of the diagnosis of the contralateral event, the last follow-up visit, or death. The reduction in risk was calculated using the following equation:

equation

with 95% confidence intervals (CIs) computed by the Poisson distribution for the number of observed events.

Although the Anderson model did not include affected male relatives (eg, father/brother/son), a woman with an affected male relative would be expected to have at least the same risk of developing a second primary breast cancer as a woman with affected female relatives. Thus we modified the Anderson criteria by including male relatives when defining pedigree type, resulting in three types of pedigrees: (1) affected parent/child, (2) affected sibling, and (3) affected second-degree relative. To classify according to type of pedigree, family history information was available from three potential sources: telephone interview, a study-specific questionnaire, and medical record. This information was used hierarchically, with family history obtained from the telephone interview considered first, and if not available, then considering questionnaire information, and lastly medical record documentation. Subjects were also classified based on whether their first primary cancer was diagnosed before or after age 50 years (pre/postmenopausal).

Observed and expected numbers of contralateral events were summed over the three pedigree types to obtain totals for each group (pre/postmenopause) adjusted for pedigree type. Similarly, totals were summed over both pedigree type and menopausal status to obtain adjusted totals for the full group.

The use of adjuvant chemotherapy or tamoxifen may also have an influence on the risk of a contralateral event. Adjuvant chemotherapy for a primary cancer was associated with a 20% reduction in contralateral breast cancer risk in the Peto overview analysis.¹² Tamoxifen has been associated with a 47% reduction in contralateral breast cancer risk.¹³ To account for these effects, the expected contralateral breast cancers were reduced by 20% for those women who received any adjuvant chemotherapy and by 47% for those women who used any adjuvant tamoxifen. For those women who had both adjuvant chemotherapy and tamoxifen, we applied the 47% risk reduction figure.

	RESULTS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Patient Characteristics
The characteristics of the 745 women who compose the current cohort are summarized in Table 1. The median age of the 745 women at first breast cancer was 49 years (range, 21 to 87 years); 41% had prophylactic subcutaneous mastectomy, and 59% had prophylactic total mastectomy. Most women (71.8%) were alive at the time of follow-up. Questionnaires were completed for 673 women (90.3%), but medical record information, including cancer occurrences and some risk factor data, are available for all women.

Pathology Review
The prophylactic mastectomy sections were available for 687 cases. Tissue was not available for 58 cases. The pathologists characterized the prophylactic mastectomy sections as follows: normal, nonproliferative change, 77%; proliferative change without atypia, 20%; atypical hyperplasia, 2.6%; carcinoma-in-situ, 0.4%; and invasive carcinoma, 0.1%. The invasive cancer that was identified during the pathologic review for this study was not identified as such at the time of prophylactic mastectomy. Of note, this patient had no evidence of breast cancer 28 years after prophylactic surgery. Three women were found to have carcinoma-in-situ on pathologic review for this study, which were not identified as such at the time of surgery. None of the women have developed breast cancer.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Women with a personal history of breast cancer who also have a positive family history have a considerably increased risk of developing a contralateral second primary. In this circumstance, some women have had bilateral mastectomy—a therapeutic procedure for the affected breast and a contralateral prophylactic procedure. In this report we describe a cohort of 745 women with both a personal and family history of breast cancer who had contralateral prophylactic mastectomy at the Mayo Clinic between 1960 and 1993. Eight women developed a contralateral new primary breast cancer despite the prophylactic mastectomy. We used the Anderson model to calculate the expected number of contralateral events in the absence of preventive surgery.^7,8 Our results support a more than 90% reduction in contralateral breast cancer risk with prophylactic surgery.

Anderson and Badzioch⁷ provide absolute risk data for contralateral breast cancer risk in women of various ages who had both a personal and family history of breast cancer. Their data are based on 556 women with breast cancer seen at the M.D. Anderson Cancer Center, all of whom had an affected relative with breast cancer. Patients were classified by menopausal status and whether or not the affected relative was their mother, sister, or a second-degree relative. These data can be used to determine the probability of a contralateral breast primary in a woman, based on her age at her first primary, her present age, and the nature of her family history. Their patients were identified starting in 1944, with the results published in 1985. Our patient cohort was identified between 1960 and 1993. Although there is considerable overlap in these two time periods, changes in adjuvant systemic therapy could impact contralateral breast cancer risk. Tamoxifen in particular has been used more commonly in the adjuvant setting since the mid-1980s. Tamoxifen has been associated with a 47% reduction of contralateral breast cancer risk.¹³ Adjuvant chemotherapy used to treat primary breast cancer has also become more common since the mid-1980s. Adjuvant chemotherapy for a primary cancer has been shown to reduce the risk of a contralateral event by 20%.¹² We applied these degrees of risk reduction to the expected breast cancer rate of the women in our cohort who had used adjuvant tamoxifen or chemotherapy. As described in our results, this adjustment for the use of adjuvant systemic therapy made minimal changes in our estimated risk reductions due to prophylactic mastectomy.

For the 388 premenopausal women who had contralateral prophylactic mastectomy in our cohort, the Anderson model predicted that 106.2 (27.4%) would have developed a contralateral primary over a median of 11 years of follow-up after their first breast cancer. The number expected in the postmenopausal group was approximately half of that, which reflects the significantly increased likelihood of an inherited predisposition in younger women who develop breast cancer and have a family history of the disease. How does the Anderson model prediction of risk of contralateral breast cancer compare with other published series? Harris et al¹ published an early series addressing this question, observing 198 women with a personal and family history of breast cancer for contralateral events. In their series, they found a 34.7% incidence of second breast cancers in these women by the end of year 16 of follow-up. A recent report by Peralta et al¹⁴ found a rate of contralateral breast cancer of 27% at 15 years in a group of 182 women, approximately half of whom had a positive family history. More recent studies focus on the level of risk among BRCA1/2 mutation carriers. Haffty et al¹⁵ documented a contralateral breast cancer risk in BRCA1/2 carriers at 5 and 10 years of 16% and 28%, respectively. Our 11-year expected risks for contralateral breast cancer of 27.4% in premenopausal women and 14.1% in postmenopausal women with both personal and family histories of breast cancer are consistent with those reported by Harris et al¹ and Peralta et al.¹⁴

In this group of 745 women, 41% underwent subcutaneous prophylactic mastectomy and 59% underwent total mastectomy. There were four post–prophylactic mastectomy breast cancers after subcutaneous mastectomy and four after total mastectomy. Thus although the risk of a new primary is markedly reduced, neither procedure is completely protective. If we see similar results with the subcutaneous mastectomy, what is the rationale for the total mastectomy in this setting? A very important consideration is the greater variability in technique with the subcutaneous procedure. The surgical team at Mayo was very aggressive in removing as much breast tissue as possible with the subcutaneous procedure; their results are not necessarily generalizable to subcutaneous procedures that would preserve more breast tissue to enhance cosmesis. Also, breast and nipple reconstruction options have improved significantly over the years, making the major rationale for the subcutaneous procedure, ie, nipple preservation, less relevant today. In this era, if a woman elects prophylactic mastectomy, the total mastectomy affords more complete tissue removal and thus represents the generally preferred procedure.

Another option to reduce contralateral breast cancer risk is tamoxifen. The 1998 Oxford meta-analysis showed that adjuvant tamoxifen for 5 years reduced contralateral breast cancer risk by 47% (95% CI, 38% to 56%).¹³ It should be noted that the tamoxifen effect seems to be restricted to women whose first breast cancer was estrogen receptor (ER)–positive. The most recent Early Breast Cancer Trialists’ update showed no effect of adjuvant tamoxifen on contralateral breast cancer risk in women with an ER-negative first breast cancer.¹⁶ Similarly, in the recently reported National Surgical Adjuvant Breast and Bowel Project B-23 trial, there was no effect on contralateral breast cancer events in women given tamoxifen whose first breast cancer was ER-negative.¹⁷

In conclusion, a woman at significantly increased risk for a contralateral breast cancer primary can consider prophylactic mastectomy to reduce her risk. When contemplating such a strategy, consideration must also be given to the woman’s risk of recurrence from her first breast cancer and her ovarian cancer risk. Ipsilateral breast conservation and tamoxifen represent another acceptable approach. Using the Anderson model to predict contralateral breast cancer risk, we have estimated a 90% reduction in the risk of second breast cancer events with contralateral prophylactic mastectomy.

	ACKNOWLEDGMENTS

 
Supported in part by grants from the Department of Defense (grant no. DAMD 17-94-J-4216) and the National Cancer Institute (grant nos. U10 CA37404-13 and ROI CA80181).

We are indebted to the participants in this study for their help in addressing an important topic. We thank Ann Harris and members of the Survey Research Center for follow-up of the patients, Randy Vrabel and John Hermans for data analysis, and Gail Prechel, Bonny Reinmuth, and Shannon Seeger for preparation of the manuscript.

	REFERENCES

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
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2. Fisher ER, Fisher B, Sass R, et al: Pathologic findings from the National Surgical Adjuvant Breast Project (Protocol No. 4): XI. Bilateral Breast Cancer. Cancer 54: 3002-3011, 1984[Medline]

3. Obedian E, Fischer DB, Haffty BG: Second malignancies after treatment of early-stage breast cancer: Lumpectomy and radiation therapy versus mastectomy. J Clin Oncol 18: 2406-2412, 2000[Abstract/Free Full Text]

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5. Verhoog LC, Brekelmans CTM, Seynaeve C, et al: Survival and tumour characteristics of breast cancer patients with germline mutations of BRCA1. Lancet 351: 316-321, 1998[Medline]

6. Robson M, Gilewski T, Haas B, et al: BRCA-associated breast cancer in young women. J Clin Oncol 16: 1642-1649, 1998[Abstract]

7. Anderson DE, Badzioch MD: Bilaterality in familial breast cancer patients. Cancer 56: 2092-2098, 1985[Medline]

8. Offit K, Brown K: Quantitating familial cancer risk: A resource for clinical oncologists. J Clin Oncol 12: 1724-1736, 1994[Abstract/Free Full Text]

9. Woods JE: Subcutaneous mastectomy: Current state of the art. Ann Plast Surg 11: 541-550, 1983[Medline]

10. Woods JE: Breast reconstruction: Current state of the art. Mayo Clin Proc 61: 579-585, 1986[Medline]

11. Bilimoria MM, Morrow M: The woman at increased risk for breast cancer: Evaluation and management strategies. CA Cancer J Clin 45: 263-278, 1995[Abstract]

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14. Peralta EA, Ellenhorn JDI, Wagman LD, et al: Contralateral prophylactic mastectomy improves the outcome of selected patients undergoing mastectomy for breast cancer. Am J Sur 180: 439-445, 2000

15. Haffty BG, Ward BA, Matloff E, et al: Patients with germline BRCA1/2 mutations treated by lumpectomy and radiation therapy (L+RT) have similar risks of ipsilateral and contralateral second primary tumors. Proc Am Soc Clin Oncol 19: 77a, 2000 (abstr 299)

16. Early Breast Cancer Trialists’ Collaborative Group: 2000 NIH Consensus Conference on Adjuvant Therapy for Breast Cancer. Http://consensus.nih.gov

17. Fisher B, Anderson S, Tan-Chiu E, et al: Tamoxifen and chemotherapy for axillary node-negative estrogen receptor-negative breast cancer: Findings from National Surgical Adjuvant Breast and Bowel Project B-23. J Clin Oncol 19: 931-942, 2001[Abstract/Free Full Text]

Submitted January 29, 2001; accepted June 1, 2001.

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