Originally published as JCO Early Release 10.1200/JCO.2006.07.3890 on December 11 2006

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Quality of Life After Contralateral Prophylactic Mastectomy in Newly Diagnosed High-Risk Breast Cancer Patients Who Underwent BRCA1/2 Gene Testing

Kenneth P. Tercyak, Beth N. Peshkin, Barbara M. Brogan, Tiffani DeMarco, Marie F. Pennanen, Shawna C. Willey, Colette M. Magnant, Sarah Rogers, Claudine Isaacs, Marc D. Schwartz

From the Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington, DC

Address reprint requests to Marc D. Schwartz, PhD, Cancer Control Program, Lombardi Comprehensive Cancer Center, Georgetown University Medical Center, 3300 Whitehaven St NW, Ste 4100, Washington, DC 20007-2401; e-mail: schwartm{at}georgetown.edu

	ABSTRACT

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PURPOSE: Recent studies indicate that high-risk breast cancer patients (ie, women who carry mutations in BRCA1/2 genes) who opt for contralateral prophylactic mastectomy (CPM) have a substantially reduced risk of developing contralateral breast cancer. However, the immediate and long-term impact of this decision on women's quality of life and psychosocial functioning is largely unknown. In this study, we compared the impact of BRCA1/2 genetic test result and CPM on these outcomes among newly diagnosed breast cancer patients who opted for CPM at the time of their definitive surgical treatment versus patients who did not.

PATIENTS AND METHODS: Participants were 149 high-risk women who underwent genetic counseling and testing for alterations in the BRCA1/2 genes. We measured self-reported quality of life, cancer-specific distress, and genetic testing–specific distress using standardized instruments before receipt of genetic test results and again 1 and 12 months later.

RESULTS: Compared with patients who chose breast conservation or unilateral mastectomy, those who chose mastectomy of the affected breast and CPM of the unaffected breast did not report diminished quality of life or elevated distress.

CONCLUSION: With respect to quality of life and distress, patients who choose CPM fare as well as those who do not in the first year after surgery.

	INTRODUCTION

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Unilateral mastectomy (UM) in combination with contralateral prophylactic mastectomy (CPM) has long been an option for newly diagnosed breast cancer patients at high risk for developing a contralateral breast cancer. Guidelines¹ describe the presence of a BRCA1 or BRCA2 (BRCA1/2) mutation as the strongest factor suggesting consideration of CPM. Breast cancer patients with a BRCA1/2 mutation have a 40% to 65% lifetime risk of developing contralateral breast cancer.^2-5 They may choose to manage this risk via surveillance, possibly in conjunction with risk-reducing measures such as tamoxifen or oophorectomy.^6,7 Alternatively, they may choose to manage their risk via CPM.^1,6,7

High-risk breast cancer patients who opt for CPM substantially reduce their risk for contralateral breast cancer.^8-10 In 2005, Herrinton et al⁸ reported a 97% decrease in the incidence of contralateral breast cancer and a 43% decrease in breast cancer mortality among patients who opted for CPM. The only study to examine the impact of CPM on survival in BRCA1/2 mutation carriers did not provide a definitive conclusion because of short follow-up and the association of CPM with prophylactic oophorectomy.¹⁰

Given the efficacy of CPM and the availability of BRCA1/2 testing, genetic testing is increasingly used by patients and physicians to guide surgical decisions among high-risk breast cancer patients.^11-14 We found that 48% of patients with positive BRCA1/2 test results opted for immediate mastectomy of the affected breast along with CPM of the unaffected breast.¹⁵ Several smaller studies have found even higher rates of CPM among carriers.^12,14

These data suggest that newly diagnosed high-risk breast cancer patients may increasingly be faced with the option of CPM. Thus, data on the psychosocial implications of CPM are critical for informed decision making in both patients and physicians.^16,17 A large retrospective cohort study found high satisfaction, little regret, and few adverse psychosocial symptoms at a mean of 10 years after CPM.¹⁸ A recent cross-sectional study¹⁹ reported comparable quality-of-life outcomes between breast cancer survivors who did and did not receive CPM. These data are consistent with studies that have examined the impact of bilateral prophylactic mastectomy among unaffected women.²⁰ Although these data are reassuring, some questions remain. Because the majority of participants in prior studies were unaware of their BRCA1/2 mutation status, the impact of CPM among mutation carriers is not clear. Furthermore, the lack of prospective studies limits conclusions about the quality-of-life impact of CPM.¹⁷

In this report, we describe the results of a prospective series of newly diagnosed breast cancer patients who underwent BRCA1/2 testing before definitive surgery. Controlling for potential confounders, we compared outcomes of patients who opted for immediate CPM versus those who did not. We were particularly interested in the impact of CPM during the immediate postdiagnostic period (1 month after testing) and after the completion of adjuvant treatment (12 months after testing).

	PATIENTS AND METHODS

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Study Population
This study was approved by the institutional review board at Georgetown University. From 1997 to 2003, patients were self-referred into the study by contacting the program directly (after a physician recommendation) or by indicating their desire to participate on a family history screening form that was distributed in the waiting room of participating surgeons at the Lombardi Cancer Center and in private practice in the Washington DC area. Eligible patients were newly diagnosed with ductal carcinoma in situ (DCIS) to stage IIIa breast cancer, had not received definitive local breast cancer treatment (ie, unilateral or bilateral mastectomy or lumpectomy plus initiation of radiation treatment),¹⁵ and met clinical criteria designed to identify individuals with a minimum 10% probability of carrying a BRCA1/2 mutation.^21-28 These criteria are described in more detail in our previous report.¹⁵ Eligible participants were informed that the study was examining the impact of genetic counseling and testing on medical decisions and quality of life and that genetic testing was an option but not a requirement for study participation.

Of 227 eligible patients, 24 (11%) declined the baseline interview, and 36 (16%) completed the interview but declined genetic testing. Differences between decliners and participants are described in a separate report.¹¹ The sample for this report was 167 women who completed a baseline interview, genetic counseling, and testing. At 1 month, follow-up data were available on 147 patients (88%), and 12-month follow-up data were available on 149 patients (89%). However, because not all patients with complete 1-month data also had complete 12-month data and vice versa, 1- and 12-month data were analyzed separately.

Procedures
Eligible patients completed a structured telephone interview that assessed sociodemographics, family history, disease characteristics, quality of life/distress, and surgical recommendations. Participants were invited to a genetic counseling session with a trained oncology nurse educator or genetic counselor. This session was comparable to traditional genetic counseling for hereditary breast cancer risk but with an added focus on risks for second breast cancers, risks and benefits of genetic testing at initial diagnosis, and efficacy of breast conservation and CPM for BRCA1/2 mutation carriers. Patients who chose testing were scheduled for a disclosure session as soon as test results were available. Disclosure sessions were delivered in person or via the telephone when requested by the participant. During the disclosure session, management options were presented along with a general discussion of the potential benefits, risks, and limitations of each. All patients were referred back to their surgeon for discussions of surgical and reconstructive procedures. Genetic counseling and testing were provided at no cost.

Participants completed follow-up interviews at 1, 6, and 12 months after disclosure of genetic test results. In this report, we focus on the 1- and 12-month assessments to evaluate the impact of CPM in the short and long term.

Measures
Sociodemographics. We assessed age (< 40 v 40 years), race (white v other), education (< college v college), marital status (unmarried v married), employment (< full time v full time), and ethnicity (Jewish v other).

Family history. We assessed the number of first- and second-degree relatives affected with breast or ovarian cancer. We compared patients with less than two affected relatives with patients with two or more affected relatives.

Disease and treatment characteristics. We abstracted TNM stage from medical records. For eight participants with missing data, we used a modal substitution (results were identical with and without the substitution). For analyses, we dichotomized stage as DCIS (0)/I versus II/IIIa. At 1 and 12 months, we classified patients as to whether they reported receiving or having received adjuvant chemotherapy.

Surgical recommendation. Patients reported whether their surgeon had recommended CPM and, if so, whether that recommendation was conditional on a positive BRCA1/2 test result. Because they did not differ on our outcome measures, we combined patients who reported either an absolute or conditional recommendation and compared them with patients who reported no recommendation.

Genetic testing result. Participants who were found to carry a BRCA1/2 mutation were classified as positive. Because none of the participants who tested negative were from families with a previously identified mutation, failure to detect a mutation or the detection of a variant of unknown clinical significance was considered an uninformative result.

Definitive surgery. Self-reported surgery decisions were confirmed from genetic counseling and medical records. Patients who had surgery to remove both the affected and contralateral breast were classified as having CPM (n = 29 at 1 month; n = 44 at 12 months). Patients who had only the affected breast removed were classified as having UM (n = 27 at 1 month; n = 33 at 12 months). Patients who reported lumpectomy were classified as having breast-conserving therapy (BCT). At 1 month, 91 patients had received a lumpectomy (not all had initiated radiation). At 12 months, 72 patients had lumpectomy and radiation. For analyses, we combined the UM and BCT groups because these groups did not differ.

Breast reconstruction. We abstracted reconstruction information from genetic counselor/medical records and patient self-report. The high rate of breast reconstruction precluded comparing participants on this variable.

Oophorectomy. At each assessment, participants reported whether they had oophorectomy. We compared patients who reported oophorectomy at the 12-month follow-up with those who did not.

Quality of life. We measured quality of life at each assessment with the total score on the 36-item Functional Assessment of Cancer Therapy–Breast (FACT-B; Cronbach's = .90).^29,30 Higher scores on this measure indicate more favorable quality of life.

Psychological distress. We measured cancer distress and genetic testing distress with the total score on the 15-item Impact of Events Scale (IES; Cronbach's = .83)³¹ and the 17-item Multidimensional Impact of Cancer Risk Assessment (Cronbach's = .91).³² Higher scores on these measures indicate higher distress.

Data Analysis
We generated descriptive statistics to characterize the sample. To identify potential confounders, we evaluated the bivariate associations of the sample characteristics with quality of life and distress outcomes at 1 and 12 months using t tests. To evaluate the impact of test result and CPM after adjusting for potential confounders, we used multiple linear regression with hierarchical variable entry.

	RESULTS

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Sample Characteristics
As displayed in Table 1, the mean age of the sample was 45 years (range, 23 to 70 years). The sample was predominantly white, college educated, married, and employed. Two thirds of the patients were diagnosed with DCIS or stage I breast cancer. At 1 month, 41% of patients had initiated chemotherapy, and 44% had received chemotherapy by 12 months. At 1 month, 20% of the sample had received a CPM, and at 12 months, 29% of the sample had received a CPM. In the overall sample,¹⁵ 48% of patients who received a positive test result opted for CPM compared with 24% of patients who received uninformative results. However, in the subset of participants who compose this sample, 54% of carriers and 25% of those who had uninformative results opted for CPM. The median time from surgery to the 1- and 12-month interviews was 36.5 days (range, 13 to 160 days) and 367.5 days (range, 119 to 552 days), respectively. Time from surgery to interview was not associated with any of our outcomes.

Quality of life. After controlling for baseline FACT-B, stage, and receipt of adjuvant chemotherapy (R² = 0.35, P < .001), neither test result (R² = 0.00, P = .96) nor CPM (R² = 0.00, P = .49) predicted short-term quality of life (Table 3). Only receipt of adjuvant chemotherapy was independently associated with quality of life (ß = –.15, P = .04).

Genetic testing–specific distress. Because this outcome measures response to genetic testing result, it was not evaluated at baseline. Genetic test result, entered on the first step, was significantly associated with genetic testing distress (R² = 0.17, P < .001). Carriers reported significantly more genetic testing–specific distress compared with patients with uninformative results (ß = .41, P < .001). Receipt of CPM was unrelated to short-term genetic testing distress (R² = 0.01, P = .11). For each of the models, exploratory analyses failed to detect an interaction between test result and receipt of CPM.

Bivariate Predictors of Long-Term Quality of Life and Distress
Women diagnosed with later stage disease (Welch-t₈₂ = 2.22, P = .03) and women who had their ovaries removed (t₁₄₇ = 2.62, P = .01) reported poorer quality of life. Women with later stage disease (Welch-t₇₄ = 3.57, P = .0006), those who received chemotherapy (t₁₂₀ = 3.52, P = .0006), those who opted for CPM (Welch-t₆₄ = 2.46, P = .02), and those who carried a BRCA1/2 mutation (Welch-t₂₄ = 2.93, P = .007) reported greater long-term genetic testing–specific distress (Table 2).

Multivariate Predictors of Long-Term Quality of Life and Distress
Quality of life. In step 1, we entered baseline FACT-B score, stage, and receipt of oophorectomy (R² = 0.35, P < .001). When entered in the next steps, neither test result (R² = 0.00, P = .29) nor CPM (R² = 0.00, P = .63) predicted quality of life (Table 4). In the final model, only oophorectomy was associated with quality of life (ß = –.15, P = .04); women who had an oophorectomy reported poorer quality of life.

Genetic testing–specific distress. After controlling for stage and receipt of adjuvant chemotherapy (R² = 0.13, P < .001), BRCA1/2 test result significantly predicted long-term distress (R² = 0.06, P = .001). Receipt of CPM was not associated with distress (R² = 0.01, P = .11). Mutation carriers (ß = .23, P = .001) and those who had received chemotherapy (ß = .17, P = .04) reported higher genetic testing distress.

We did not detect any interactions between test result and surgery decision in any of the models. In parallel analyses in which we controlled for quality of life and distress at 1 month (instead of at baseline), we found the same pattern of results as described earlier.

	DISCUSSION

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There is accumulating evidence that CPM is an effective strategy for managing contralateral breast cancer risk among BRCA1/2 mutation carriers. Offering BRCA1/2 testing to newly diagnosed high-risk patients allows them to consider the potential benefits of immediate bilateral mastectomy. Recent studies suggest that 50% or more of new breast cancer patients who carry a BRCA1/2 mutation opt for prophylactic mastectomy of the unaffected breast.^12,15 However, to adequately counsel newly diagnosed patients, data addressing the psychosocial impact of CPM are critical.

This study is the first to prospectively evaluate the impact of CPM among newly diagnosed breast cancer patients. Compared with patients who chose UM or BCT, those who chose CPM did not exhibit diminished quality of life or elevated distress. These results are consistent with earlier studies reporting high satisfaction, low regret, and no evidence of increased psychosocial symptoms.¹⁸ This study compliments and extends previous studies by using a prospective design, incorporating a comparison group of patients who did not opt for CPM, and focusing on breast cancer patients who underwent BRCA1/2 testing at the time of their initial diagnosis. Taken together, these studies suggest that patients who choose CPM fare as well as those who do not in the short and long term.

Key determinants of dissatisfaction with CPM identified in previous research were receipt of reconstruction and the need for additional breast surgery.¹⁸ We could not evaluate this in the present study because of our sample's high rate of reconstruction and our failure to assess surgical complications. However, given our relatively short follow-up period, there were likely few, if any, resurgeries. Thus, concerns remain about the impact of reconstruction and resurgery on long-term quality of life after CPM. In previous research among women without breast cancer, physician recommendation to obtain prophylactic bilateral mastectomy was associated with decreased satisfaction with that decision.²⁰ We did not find an association between physician CPM recommendation and quality of life. It is possible that the process of genetic counseling and the receipt of BRCA1/2 test results led patients to perceive a more active decision-making process. This may have led to higher overall satisfaction and quality of life.³³ It is also possible that preference for CPM may be high among many newly diagnosed high-risk breast cancer patients. Thus, a physician recommendation for CPM may be consistent with patient preferences in this setting.

Although CPM did not predict quality of life or distress, several other variables did. Consistent with previous research, TNM stage and receipt of adjuvant chemotherapy were associated with poorer quality of life.^34,35 Although prophylactic oophorectomy was associated with poorer long-term quality of life, caution is needed in interpreting this finding because few women opted for prophylactic oophorectomy. That genetic test result did not predict quality of life or distress is consistent with prior research among breast cancer survivors.²⁷ Patients who received positive genetic test results did report higher levels of genetic testing–specific distress. These findings suggest that the Multidimensional Impact of Cancer Risk Assessment³² may be particularly sensitive to the impact of genetic testing. Previous researchers have raised questions about the sensitivity of measures such as the IES in this population.³⁶

Although we found no adverse impact of CPM after presurgical genetic testing, our data do not address the impact of presurgical testing itself. There have been questions about genetic testing among newly diagnosed patients because of concerns about feasibility,³⁷ surgical delay,³⁸ and psychological distress.³⁹ Prior reports^11-13,15,40 suggest that patients will use BRCA1/2 genotype information to help guide their surgical decision making. However, additional research is needed to definitively determine the psychosocial and quality-of-life impact of rapid genetic counseling.

Although this is the largest prospective sample to date of women who underwent genetic testing before definitive surgery, the limited number of patients who chose CPM raises issues of power. These results should be interpreted cautiously as indicating that there was not a large adverse impact of CPM on psychosocial outcomes. The generalizability of these results may be limited by the well-educated, affluent, predominantly white sample and the provision of free genetic testing and telephone-based disclosures. Furthermore, given the high rates of breast reconstruction, it was impossible to distinguish alterations in quality of life and distress that may have been related to reconstruction or surgical complications. The variable range between final surgery and each of the follow-up interviews is also a limitation. Future studies should key the interviews to the date of diagnosis to ensure more uniformity in interview timing. Finally, because of missing follow-up data, the sample in the 1-month analyses differed slightly from the 12-month sample, precluding direct comparisons of 1- and 12-month outcomes.

In conclusion, this report provides the first prospective evidence that newly diagnosed breast cancer patients who opt for CPM report comparable psychosocial outcomes to patients who choose UM or BCT. These findings may be useful in informing patient decisions about genetic testing at the time of diagnosis and the types of medical management options most consistent with patients' goals and values.

	AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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The authors indicated no potential conflicts of interest.

	AUTHOR CONTRIBUTIONS

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Conception and design: Beth N. Peshkin, Claudine Isaacs, Marc D. Schwartz

Financial support: Marc D. Schwartz

Administrative support: Sarah Rogers, Marc D. Schwartz

Provision of study materials or patients: Barbara M. Brogan, Tiffani DeMarco, Marie F. Pennanen, Shawna C. Willey, Colette M. Magnant, Claudine Isaacs, Marc D. Schwartz

Collection and assembly of data: Beth N. Peshkin, Barbara M. Brogan, Tiffani DeMarco, Sarah Rogers, Claudine Isaacs, Marc D. Schwartz

Data analysis and interpretation: Kenneth P. Tercyak, Beth N. Peshkin, Marc D. Schwartz

Manuscript writing: Kenneth P. Tercyak, Beth N. Peshkin, Claudine Isaacs, Marc D. Schwartz

Final approval of manuscript: Kenneth P. Tercyak, Beth N. Peshkin, Barbara M. Brogan, Tiffani DeMarco, Marie F. Pennanen, Shawna C. Willey, Colette M. Magnant, Claudine Isaacs, Marc D. Schwartz

	ACKNOWLEDGMENTS

 
We thank Caryn Lerman, Theodore Tsangaris, David Main, Clinton Finch, William Lawrence, Chanita Hughes Halbert, Lisa Moss, Sarah Kelleher, and Caroline Kim for their contributions to this research.

	NOTES

 
published online ahead of print at www.jco.org on December 11, 2006.

Supported by National Institutes of Health Grants No. R01CA074861 (M.D.S.) and K07CA091831 (manuscript preparation; K.P.T.).

Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.

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Submitted May 14, 2006; accepted October 24, 2006.

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