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Breast Cancer after Augmentation: Oncologic and Reconstructive Considerations among Women Undergoing Mastectomy

Cho, Eugenia H. B.S.; Shammas, Ronnie L. B.S.; Phillips, Brett T. M.D., M.B.A.; Greenup, Rachel A. M.D., M.P.H.; Hwang, E. Shelley M.D., M.P.H.; Hollenbeck, Scott T. M.D.

Plastic & Reconstructive Surgery: June 2017 - Volume 139 - Issue 6 - p 1240e–1249e
doi: 10.1097/PRS.0000000000003342
Breast: Original Articles
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Background: Breast augmentation with subglandular versus subpectoral implants may differentially impact the early detection of breast cancer and treatment recommendations. The authors assessed the impact of prior augmentation on the diagnosis and management of breast cancer in women undergoing mastectomy.

Methods: Breast cancer diagnosis and management were retrospectively analyzed in all women with prior augmentation undergoing therapeutic mastectomy at the authors’ institution from 1993 to 2014. Comparison was made to all women with no prior augmentation undergoing mastectomy in 2010. Subanalyses were performed according to prior implant placement.

Results: A total of 260 women with (n = 89) and without (n = 171) prior augmentation underwent mastectomy for 95 and 179 breast cancers, respectively. Prior implant placement was subglandular (n = 27) or subpectoral (n = 63) (For five breasts, the placement was unknown). Breast cancer stage at diagnosis (p = 0.19) and detection method (p = 0.48) did not differ for women with and without prior augmentation. Compared to subpectoral augmentation, subglandular augmentation was associated with the diagnosis of invasive breast cancer rather than ductal carcinoma in situ (p = 0.01) and detection by self-palpation rather than screening mammography (p = 0.03). Immediate two-stage implant reconstruction was the preferred reconstructive method in women with augmentation (p < 0.01).

Conclusions: Breast cancer stage at diagnosis was similar for women with and without prior augmentation. Among women with augmentation, however, subglandular implants were associated with more advanced breast tumors commonly detected on palpation rather than mammography. Increased vigilance in breast cancer screening is recommended among women with subglandular augmentation.

CLINICAL QUESTION/LEVEL OF EVIDENCE: Therapeutic, III.

This and Related “Classic” Articles Appear on Prsjournal.Com for Journal Club Discussions.

Durham, N.C.; and Philadelphia, Pa.

From the Divisions of Plastic and Reconstructive Surgery and Advanced Oncologic and Gastrointestinal Surgery, Duke University Health System; and the Department of Bioengineering, University of Pennsylvania.

Received for publication October 19, 2016; accepted December 7, 2016.

A “Hot Topic Video” by Editor-in-Chief Rod J. Rohrich, M.D., accompanies this article. Go to PRSJournal.com and click on “Plastic Surgery Hot Topics” in the “Digital Media” tab to watch. On the iPad, tap on the Hot Topics icon.

Disclosure: The authors have no financial interest to declare in relation to the content of this article.

Scott T. Hollenbeck, M.D., Division of Plastic and Reconstructive Surgery, Duke University Medical Center, Box 3945, Durham, N.C. 27710, scott.hollenbeck@duke.edu

Breast augmentation is the most common cosmetic surgical procedure in the United States, with nearly 300,000 women undergoing augmentation annually.1 Breast cancer affects one in eight American women and remains the second most common cancer diagnosis among women nationwide.2 Current national incidence rates predict that among women undergoing breast augmentation each year, approximately 35,000 will eventually be diagnosed with breast cancer and seek treatment and reconstructive options. Identifying key considerations in the early detection, diagnosis, and management of breast cancer in augmented women is important for improving risk counseling and decision making in this patient population.

The safety of breast implants has been thoroughly investigated in recent decades, with epidemiologic evidence showing no link between implants and the risk of developing breast cancer.3–12 Nevertheless, concerns remain that implants may delay the early mammographic detection of breast cancer and thus possibly lead to worse prognosis.10,11,13,14 Specifically, subglandular implants are reported to obscure the visualization of at least 39 percent of breast tissue, whereas subpectoral implants may obscure up to 28 percent of tissue.15,16 Evidence is mixed on whether breast cancer presentation differs among women with and without prior augmentation, with some studies reporting more advanced disease in the augmented cohort15,17–19 and other studies showing no difference.3,5,7,11,12 Furthermore, only one study to date has compared breast cancer stage distribution and reconstructive options following subglandular versus subpectoral implant placement, with inconclusive results because of small study sample size.20 The continued popularity of breast augmentation, coupled with the prevalence of breast cancer, underscores the importance of assessing the oncologic risks of subglandular versus subpectoral augmentation. In addition, evolving patterns in mastectomy use and immediate implant-based reconstruction highlight the need for outcomes data assessing the clinical implications of prior implant placement in postmastectomy breast reconstruction. The purpose of our study was to assess the detection, diagnosis, and management of breast cancer among mastectomy patients with a history of breast augmentation, with specific attention to prior implant placement.

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PATIENTS AND METHODS

Following institutional review board approval, a retrospective review was conducted on all women with a history of prior breast augmentation who underwent therapeutic mastectomy for breast cancer at Duke University Health System from 1993 to 2014 (n = 89). Patients were included if they had cosmetic bilateral breast augmentation before the diagnosis of invasive or in situ breast cancer. Women with prior augmentation were compared to a control group of all women aged 70 years or younger with no history of augmentation who were newly diagnosed with invasive or in situ breast cancer and underwent therapeutic mastectomy in 2010 (n = 171). This 2010 mastectomy cohort was selected as the concurrent control group because the median year of mastectomy in the augmentation cohort was 2010 ± 4 years.

Women with and without prior augmentation were compared with respect to patient characteristics at the time of mastectomy, detection method, stage at diagnosis, cancer treatment variables, and reconstructive surgery undergone. Patient demographic variables included age, body mass index, race, age at menarche, and parity. Breast cancer stage at diagnosis was coded according to the AJCC Cancer Staging Handbook, 7th edition, published by the American Joint Commission on Cancer.21 Cancer detection method was classified as either self-palpation or screening mammography. Treatment variables included the receipt of neoadjuvant or adjuvant chemotherapy, radiation therapy, and unilateral or bilateral mastectomy. Postmastectomy breast reconstruction was categorized as follows: no reconstruction, implant-based reconstruction, autologous tissue reconstruction, or combined implant and autologous tissue reconstruction. Reconstruction was considered immediate if performed concurrent with the mastectomy procedure, and delayed if performed after the mastectomy procedure. All variables were analyzed on a per-breast basis.

Among women with prior augmentation, data were collected on previous implant placement (i.e., subglandular or subpectoral), volume, type (i.e., saline or silicone), date of the primary augmentation procedure, elapsed time from augmentation surgery to breast cancer diagnosis, and the timing of implant removal from cancer-affected and contralateral breasts. Breasts with prior subglandular versus subpectoral augmentation were compared with respect to other augmentation factors, patient demographics at mastectomy, breast cancer diagnosis and detection method, treatment, and surgical and reconstructive variables. Pathology records were reviewed to obtain data on surgical margins following mastectomy, and were classified as positive (ink on tumor), close (tumor ≤2 mm of excised margin), or clear (>2 mm).

Patients choosing implant reconstruction were candidates for one-stage reconstruction if they wished to keep their current breast size or downsize to a smaller implant size. The decision to perform one-stage reconstruction was made intraoperatively after mastectomy based on the quality of the remaining implant capsule and overlying breast skin envelope. Patients who were not candidates for one-stage reconstruction were offered two-stage reconstruction with tissue expanders. Among reconstructed breasts, the following complications were assessed: nipple-areola complex necrosis requiring débridement, mastectomy skin flap necrosis requiring surgical intervention, infection requiring intravenous antibiotics, and implant loss secondary to reconstructive complications requiring an unplanned return to the operating room. Additional procedures were recorded, including nipple excision because of positive cancer margins, capsulectomy for capsular contracture, and fat grafting.

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Statistical Analysis

Bivariate statistical analyses were performed using Fisher’s exact or chi-square tests for categorical variables and the Mann-Whitney U and unpaired t tests for continuous variables. Multivariable logistic regression models of significant variables derived from bivariate analyses (p < 0.05) were used to identify variables that were independently associated with reconstructive outcomes. All tests were two-sided, with statistical significance assigned to values of p < 0.05. Statistical analyses were performed using R software, version 3.0 (The R Foundation for Statistical Computing, Vienna, Austria).

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RESULTS

A total of 89 women with a history of breast augmentation underwent therapeutic mastectomy for 95 breast cancers, with a mean follow-up of 3.6 ± 3.6 years. Details of prior augmentation surgery are summarized in Figure 1. Prior implant placement was subglandular in 27 cancer-affected breasts (28 percent) and subpectoral in 63 cancer-affected breasts (66 percent) (For five breasts, the placement was unknown). An increasing trend was observed in the number of breast cancers according to the year of augmentation procedure (p < 0.01). The stage distribution of breast cancer at diagnosis was as follows: ductal carcinoma in situ, n = 22 (23 percent); stage I, n = 34 (36 percent); stage II, n = 24 (25 percent); stage III, n = 8 (8 percent); and unknown stage, n = 7 (7 percent). Breast cancer was commonly detected by self-palpation in 45 patients (47 percent) or screening mammography in 35 patients (37 percent). The mean elapsed time from augmentation surgery to breast cancer diagnosis was 13.8 ± 10.7 years.

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Comparison of Women with and without Prior Augmentation

Women with prior augmentation were compared to a control cohort of 171 women aged 70 years or younger with no prior augmentation who underwent therapeutic mastectomy for 179 primary breast cancers in 2010. Mean follow-up was 3.8 ± 3.6 years. At the time of mastectomy, women with prior augmentation were younger (age, 51.9 ± 10.6 years versus 54.8 ± 9.9 years; p = 0.03), leaner (body mass index of 24.9 ± 5.0 kg/m2 versus 28.9 ± 7.1 kg/m2; p < 0.01), and more likely to report white race [89 percent (n = 85) versus 74 percent (n = 132); p < 0.01], compared with the no-augmentation group. No differences were noted between the two groups with respect to clinical American Joint Commission on Cancer stage at diagnosis (p = 0.19), primary tumor size (p = 0.10), number of positive nodes (p = 0.10), cancer detection method (p = 0.48), or the receipt of chemotherapy (p = 0.08) or radiation therapy (p = 0.42).

Surgical and reconstructive management variables were compared in women with and without prior augmentation. Although unilateral mastectomies were more common overall, bilateral mastectomy rates were higher in the augmentation group compared with no-augmentation patients [n = 38 (41 percent) versus n = 32 (19 percent); p < 0.01]. Postmastectomy reconstruction using implant-based methods was more commonly performed in the augmentation group compared with the no-augmentation group [n = 65 (83 percent) versus n = 32 (52 percent); p < 0.01]. No difference was noted in the timing of reconstruction [n = 51 (65 percent) immediate in the augmentation group versus n = 34 (55 percent) immediate in the no-augmentation group; p = 0.29]. Among implant-based reconstructions, immediate tissue expander placement was the preferred reconstructive approach for both groups. The augmentation group was significantly less likely to undergo autologous tissue reconstruction compared with other reconstructive approaches (p < 0.01).

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Subglandular versus Subpectoral Implant Placement

Breast cancer presentation and management were analyzed according to subglandular versus subpectoral implant placement. Implant placement was not associated with other augmentation factors, including implant size (p = 0.73), type (p = 0.87), decade of augmentation surgery (p = 0.81), and elapsed time from augmentation surgery to cancer diagnosis (p = 0.25) (Table 1). Subglandular augmentation was associated with the diagnosis of stage I to III invasive breast cancer (p = 0.01) and invasive primary tumors (p = 0.03), compared with subpectoral augmentation (Table 2). Breast cancers diagnosed after subglandular augmentation were more frequently detected by self-palpation than by screening mammography (p= 0.03). The two groups did not differ with respect to patient demographics or medical treatment variables.

A comparison of surgical and reconstructive management variables is shown in Table 3. Although two-stage tissue expander reconstruction was the overall preferred reconstructive method, subglandular augmentation was associated with higher rates of one-stage implant reconstruction (p = 0.04), compared with subpectoral augmentation. Prior implant placement was not associated with mastectomy laterality (p = 0.08), use of nipple-sparing mastectomy (p = 0.42), presence of positive surgical margins (p = 0.51), postmastectomy reconstruction rates (p = 0.22), reconstructive modality (p = 0.55), or timing of reconstruction (p = 0.60). Immediate implant-based reconstruction was most commonly performed in both augmentation groups, with no differences noted in the use of partial versus total muscle coverage (p = 0.76).

All 95 cancer-affected augmented breasts underwent removal of the previously placed implant at a mean interval of 15.1 ± 10.6 years after the primary augmentation procedure. In cancer-affected breasts, 87 prior implants (92 percent) were removed at the time of mastectomy, with the remaining eight (8 percent) removed at the final reconstruction stage. In contralateral breasts, 38 prior implants (40 percent) were removed at mastectomy, 40 (42 percent) were retained at mastectomy and removed at the final reconstruction stage, and 17 (18 percent) were not removed at mastectomy or reconstruction. Implant rupture at the time of removal was noted in eight cancer-affected breasts (8 percent) and 14 contralateral breasts (15 percent). No differences were observed in the surgical management of prior implants with regard to their placement.

Following reconstruction, prior subglandular augmentation was correlated with higher rates of infection requiring intravenous antibiotic treatment (p = 0.02) and implant loss secondary to reconstructive complications (p = 0.02) compared with subpectoral augmentation (Table 4). All three cases complicated by implant loss were bilateral implant reconstructions performed with partial muscle coverage and acellular dermal matrix support in subglandular augmented breasts; two of these cases (67 percent) were immediate one-stage reconstructions followed by postoperative radiation therapy. Bivariate analysis of selected factors associated with failed implant-based reconstruction is shown in Table 5. None of the following variables included in logistic regression analysis were independently associated with postoperative implant loss: subglandular augmentation (p = 0.48; OR, 3.00; 95 percent CI, 0.14 to 62.48), immediate one-stage reconstruction (p = 0.14; OR, 0.28; 95 percent CI, 0.05 to 1.52), and partial muscle coverage and acellular dermal matrix support (p = 0.43; OR, 9756.22; 95 percent CI, 0.00 to not applicable) (Table 6).

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DISCUSSION

This study is the largest comprehensive analysis of mastectomy for breast cancer among women with a history of breast augmentation and uniquely examines the oncologic risks of subglandular versus subpectoral implant placement. Although prior breast augmentation did not delay breast cancer diagnosis, subglandular implant placement was associated with the clinical detection of invasive, as opposed to in situ, breast tumors in comparison with subpectoral implant placement. Current evidence is lacking on whether breast augmentation in the subglandular or subpectoral plane impacts the clinical management of breast cancer at any point from primary diagnosis to reconstructive outcome. Assessing the oncologic and reconstructive risks of subglandular versus subpectoral augmentation is important in light of current national breast augmentation rates1 and breast cancer incidence,2 along with rising trends in bilateral mastectomy and immediate implant-based reconstruction.22–24 This study demonstrates the potential benefit of subpectoral augmentation over subglandular augmentation with regard to mammographic screening effectiveness, and highlights reconstructive considerations to assist with preoperative risk counseling and perioperative decision making for these patients.

The overall stage distribution of breast cancer at diagnosis was similar for women with and without prior breast augmentation, with no differences in primary tumor size or nodal status. Our staging data add to the weight of evidence demonstrating no delay in breast cancer diagnosis after augmentation.3,5,7,11,12 Existing controversy in the literature regarding breast cancer stage presentation in previously augmented breasts has been attributed to low statistical study power and study methodologic differences in the selection of control data for cohort comparison.14 It should be noted that our study did not adjust for younger age or lower body mass index in the augmentation group, factors that may underestimate the measure of association between prior augmentation and delayed breast cancer diagnosis.19 In general, however, augmented women diagnosed with breast cancer tend to be younger and leaner, and may be more breast aware, seeking medical care more quickly for breast changes or symptoms.25,26 Routine screening mammography using both implant displacement and compression views is essential for proper visualization of breast tissue in these patients.27,28 In addition, increased vigilance is warranted in women who develop capsular contracture, which is reported to reduce mammographic sensitivity by 30 to 50 percent.29 Our results add to the strong evidence base indicating that women with prior augmentation are not at increased risk of delayed breast cancer diagnosis in comparison with the general female population.

Subglandular implant placement in our series was associated with the diagnosis of invasive breast cancers detected by self-palpation rather than screening mammography. Our data underscore the need for increased vigilance in breast cancer screening among women with subglandular implants. One study to date has evaluated breast cancer diagnosis and detection method according to implant placement. Spear et al., in their retrospective series of 32 breasts reconstructions following augmentation, noted a clinically significant trend toward reduced mammographic cancer detection with subglandular augmentation compared with subpectoral augmentation, although this did not reach statistical significance.20 Subglandular implants are reported to obscure the mammographic visualization of at least 39 percent of breast tissue compared with 28 percent of tissue with subpectoral implants,15,16 with minor improvement provided by the use of displacement techniques in most patients.5,29 Importantly, mammographic sensitivity is most significantly reduced by the presence of Baker grade III or IV capsular contracture, which can obscure approximately 50 percent of breast tissue and is more common with subglandular implants.30 Of note, it is speculated that breast implants, especially in the subglandular position, may facilitate the detection of palpable breast tumors by providing a base against which to palpate.31 However, this possibility does not account for our findings that women with subglandular augmentation were diagnosed with more invasive breast cancers, compared with ductal carcinoma in situ. The apparent compromise in mammographic screening efficacy for women with subglandular implants may be related to higher rates of capsular contracture compared with subpectoral implants.16 As screening mammography remains the most important tool available for detecting early-stage curable breast cancer, it is critical to understand factors that may impair mammographic sensitivity in the augmentation population. Current guidelines for breast cancer screening provided by the 2016 U.S. Preventative Services Task Force recommend biennial screening mammography for women aged 50 to 74 years (grade B, indicating a high certainty that the net benefit is substantial).32 Current guidelines for breast self-examination are derived from the 2009 U.S. Preventative Services Task Force recommendations, which recommend against teaching breast self-examination in all women (grade D, indicating a moderate or high certainty that self-examinations have no net benefit).33 These U.S. Preventative Services Task Force recommendations apply to asymptomatic women aged 40 years or older who are not at high risk for breast cancer, and clinicians should individualize decision making to the specific patient. Our findings highlight the need for heightened vigilance in routine breast screening examinations among women with subglandular implants. Mammographic sensitivity should be a factor considered by the patient and plastic surgeon when selecting the optimal pocket plane for primary breast augmentation. Subpectoral augmentation should be favored for women at increased risk of breast cancer who are considering breast augmentation.

Immediate implant-based reconstruction has been established as a safe and reliable method of breast reconstruction across various mastectomy techniques in the setting of prior augmentation.34–37 As we observed, women with prior augmentation commonly undergo implant-based reconstruction because of limited donor tissue availability for autologous reconstructive options.38,39 Prior breast augmentation may serve as a delay procedure and potentially facilitate immediate breast reconstruction by expanding the breast skin envelope and improving blood flow to the mastectomy flap.40 In our experience, immediate two-stage breast reconstruction with tissue expanders is the preferred reconstructive method in augmentation patients, as it places less initial pressure on mastectomy flaps and provides an opportunity for minor revisions during the second stage. If a subpectoral augmentation pocket was used, the anterior capsule can be left intact and a capsulotomy can be performed to permit the insertion of a tissue-expander. If a subglandular pocket was used, a capsulectomy is commonly performed and a neosubpectoral pocket is created for implant reconstruction with acellular dermal matrix support if required. Notably, we found that immediate one-stage implant reconstruction with partial muscle coverage was more commonly performed in subglandular augmented breasts and associated with a higher risk of postoperative implant loss. It is unclear based on our data whether the capsulectomy procedure performed in women with subglandular augmentation is responsible for the complications reported. The decision to perform one-stage reconstruction was based on key clinical factors (e.g., the quality of the remaining implant capsule and overlying breast skin envelope) that were not captured in this study. Further study is warranted to determine the suitability and risks of immediate one-stage reconstruction in the setting of prior subglandular versus subpectoral augmentation.

This study has limitations, many of which are inherent in its retrospective design. First, we compared two cohorts of women with different baseline characteristics and inherent selection bias. Women who choose to undergo breast augmentation represent a unique patient population whose physical characteristics, such as lower body mass index, may be associated with different baseline breast cancer risk. Second, we were unable to collect data on the presence and grade of capsular contracture at the time of breast cancer diagnosis among augmentation patients, which may be related to implant placement and independently associated with breast cancer stage presentation, detection method, and reconstructive options and outcomes. In addition, our analysis of implant reconstructive complications in augmented women should be interpreted with caution. The small sample size of augmented women undergoing implant reconstruction may significantly overestimate the effect measure reported in logistic regression.41 Finally, our augmentation series spans a 20-year period and may be prone to evolving patterns in patient selection and practice not captured herein.

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CONCLUSIONS

This institutional series is the largest observational study of breast cancer detection, diagnosis, and management in augmented patients with respect to implant position. The stage distribution of breast cancer at diagnosis was similar in women with and without prior augmentation. Among augmented women, however, subglandular implant placement was associated with more advanced breast tumors, which were more likely to be detected on palpation than by screening mammography. Our findings underscore the need for increased vigilance in breast cancer screening among women with subglandular augmentation and should guide preoperative risk counseling and pocket plane selection for breast augmentation among women at increased risk of breast cancer.

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ACKNOWLEDGMENTS

The authors thank Gregory S. Georgiade, M.D., and Michael R. Zenn, M.D., M.B.A., who contributed to the management of patients in this study.

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