Accepted Manuscript Oncoplastic Reduction Mammaplasty, An Effective and Safe Method of Breast Conservation Angelena Crown, MD, Nicketti Handy, MD, Flavio G. Rocha, MD, Janie W. Grumley, MD PII:
S0002-9610(17)31663-X
DOI:
10.1016/j.amjsurg.2018.02.024
Reference:
AJS 12813
To appear in:
The American Journal of Surgery
Received Date: 20 November 2017 Revised Date:
23 February 2018
Accepted Date: 26 February 2018
Please cite this article as: Crown A, Handy N, Rocha FG, Grumley JW, Oncoplastic Reduction Mammaplasty, An Effective and Safe Method of Breast Conservation, The American Journal of Surgery (2018), doi: 10.1016/j.amjsurg.2018.02.024. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Oncoplastic Reduction Mammaplasty, An Effective and Safe Method of Breast Conservation
Angelena Crown, MD; Virginia Mason Medical Center, Department of General, Thoracic and Vascular Surgery, Seattle, Washington.
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Nicketti Handy, MD; Virginia Mason Medical Center, Department of General, Thoracic and Vascular Surgery, Seattle, Washington. Flavio G. Rocha, MD; Virginia Mason Medical Center, Department of General, Thoracic and Vascular Surgery, Seattle, Washington.
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Janie W. Grumley, MD (corresponding author); Virginia Mason Medical Center, Department of General, Thoracic and Vascular Surgery, Seattle, Washington. 206-223-6633,
[email protected]
INTRODUCTION: Oncoplastic breast conserving surgery (BCS) can enhance both cosmetic and oncologic breast cancer outcomes. This study evaluates the outcomes and complications associated with oncoplastic reduction mammaplasty performed by surgical breast oncologists. METHODS: A single institution retrospective chart review of patients undergoing oncoplastic reduction mammaplasty by a surgical breast oncologist for the treatment of breast cancer.
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RESULTS: Seventy-one patients were identified. The average patient age was 59.6 years (range 37-77 years). Average lesion span was 31.4 mm (range 3-166 mm). Six (8.5%) patients required additional surgery to obtain adequate margins. One (1.4%) patient developed recurrent disease during the follow-up interval. No major surgical complications were observed.
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CONCLUSION: Oncoplastic reduction mammaplasty is associated with low rates of re-excision and complications and can be safely and effectively performed by appropriately trained surgical breast oncologists.
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INTRODUCTION Breast conserving therapy (BCT) comprises partial mastectomy, axillary staging, and adjuvant systemic and radiation therapy. Seminal randomized studies have shown equivalent
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disease-free and overall survival with low risk of local recurrence that is comparable to
mastectomy. As a result, BCT has become standard of care for the treatment of early stage breast cancer.1-4
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Successful BCT requires wide local resection with the goal of attaining adequate
oncologic margins, which can compromise breast cosmesis and functionality. In fact, studies
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have shown that up to 40% of patients undergoing BCT have poor cosmetic outcomes. 5 Additionally, recent studies have suggested that up to 40% of patients with breast cancer have macromastia, which is associated with increased rates of poor cosmetic outcomes attributed to increased rates of asymmetry, tissue retraction, and radiation changes.6
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Oncoplastic surgery, which incorporates plastic surgical approaches at the time of partial mastectomy, has emerged as an alternative approach to breast conserving surgery.7 Because these tissue rearrangement techniques allow for larger resections, oncoplastic surgery has
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expanded the indications for breast conservation, allowing many patients with large or multifocal cancers who may have traditionally been advised to undergo mastectomy to consider BCT.7-9
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Larger tissue resections also allow for wider margins; as a result, oncoplastic surgery has been shown to reduce rates of inadequate surgical margins, which results in fewer re-excisions and mastectomies compared to traditional partial mastectomy.10-12 Adjuvant therapies can then be initiated more expeditiously by avoiding additional operations.13 Given the multitude of benefits, interest in oncoplastic surgery has increased over the course of the last decade.14-16
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The panoply of oncoplastic techniques ranges from simple volume redistribution techniques, including radial ellipse and mastopexy, to more advanced tissue rearrangement schemes such as reduction mammaplasty and contralateral procedures for symmetry.17 The more
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advanced techniques frequently require a multidisciplinary approach wherein a surgical breast oncologist resects the cancer and a plastic surgeon performs the tissue rearrangement component of the operation.18 Because oncoplastic surgery involves tissue rearrangement and may also
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include procedures on the contralateral breast for symmetry, there is concern that oncoplastic surgery may expose patients to additional surgical risks and complications. It has also been
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suggested the oncoplastic surgery may impair the accuracy of adjuvant radiation therapy targeting by making the localization of the tumor bed more challenging.13 Despite the ability to perform large resections, inadequate margins may still be found on final pathology. Critics of oncoplastic surgery raise concerns about the ability to accurately
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perform re-excision after oncoplastic surgery since traditionally tissue rearrangement and complex closure is typically performed by a plastic surgeon after cancer resection. As a result, there is rising interest among surgical breast oncologists to seek additional training in order to
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perform not only the cancer resection, but also the reconstruction to improve both oncologic and cosmetic outcomes.
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This study reports the oncologic and cosmetic outcomes for patients undergoing
oncoplastic reduction mammaplasties performed by surgical breast oncologists. METHODS
Oncoplastic reduction mammaplasty performed by surgical breast oncologists is routinely
offered to patients for treatment of breast cancer at Virginia Mason Medical Center in Seattle, WA. This study assesses the oncologic and cosmetic outcome of seventy-one consecutive patients who were treated by two surgical breast oncologists using this approach. The study was
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approved by the institutional review committee and met the guidelines of the responsible governmental agency. All patients undergoing oncoplastic reduction mammaplasty at Virginia Mason Medical Center from December 2012 to July 2015 were reviewed. Standard preoperative
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imaging work up included mammogram, ultrasound, and breast MRI, when indicated.
Candidacy for BCT via reduction mammaplasty was determined by the surgical breast oncologist based on imaging studies, clinical exam, and patient desire for BCT. There were no explicit
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exclusion criteria. Patients who were motivated for breast conserving surgery were offered a range of oncoplastic surgical approaches. BMI, smoking status, comorbidities, and breast size
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did not influence the surgical options offered. All patients undergoing oncoplastic reduction mammoplasty were included in this study. A multidisciplinary team comprising surgical breast oncologists, breast radiologists, radiation oncologists, and medical oncologists reviewed all patients and determined adjuvant treatment recommendations in a multi-disciplinary conference.
component of BCT.
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All patients were counseled to undergo appropriate adjuvant radiation therapy as an integral
Options for radiation therapy included standard whole breast external beam radiation as
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well as intraoperative radiation therapy under the institution’s intraoperative radiation therapy (IORT) research protocol. Patients age 45 and older with unifocal tumors 3 cm or smaller on
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pre-operative imaging, no clinical evidence of nodal disease, and no lymphovascular invasion on core needle biopsy were offered intraoperative radiation therapy. Patients who elected to undergo IORT received 20Gy of radiation directly in the partial mastectomy cavity at the time of oncoplastic reduction mammaplasty. Preoperative marking for wise-pattern reductions was performed by the operating surgical breast oncologists (Figure 1). Wise-pattern reductions were carried out by
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circumscribing the nipple-areolar complex and defining an appropriate pedicle to ensure adequate blood supply to the nipple-areolar complex. Partial mastectomies were performed through the wise-pattern incisions as was the sentinel lymph node biopsy, when indicated.
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Additional tissue resection was completed as necessary to allow for closure of the wise-pattern reduction. All specimens removed were sterilely inked by the surgeon and submitted for
pathologic review. The tumor cavity was circumferentially marked with surgical clips to allow
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for detection of the tumor bed on subsequent imaging and targeting for adjuvant radiation therapy. Specimen radiograph and pathologic gross evaluation were performed to assess
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margins intraoperatively. No drains were placed. Patients were admitted for overnight observation post-operatively and discharged to home on post-operative day one. Margins were considered adequate if margins were greater than 2mm. All patients with inadequate margins were advised to undergo re-excision unless the inadequate margin was chest wall. All patients
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were seen within two weeks of their operation and as needed for management of complications. Patients were seen for clinical follow up every six months for the first two years then annually thereafter. Cosmesis scores were assigned by the clinician according to an objective list of
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criteria at six months (Table 1) Complications and associated interventions were identified through chart review as well as from the prospectively collected data in the Virginia Mason
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Multidisciplinary Breast Cancer Database. They were classified using the standard ClavienDindo scale.19
Pearson’s chi-squared tests were used for comparison of categorical variables and
unpaired t-tests were used for comparison of continuous variables. Unadjusted logistical regression was performed using MedCalc version 12.7.5. P-values less than or equal to 0.05 were considered statistically significant.
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RESULTS Seventy-one patients underwent oncoplastic reduction mammaplasty (Table 2). The average patient age was 59.6 years (range 37-77) and the average BMI was 31.9 kg/m2 (range
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18-42). Thirty-five (49.3%) patients had BMIs greater than 30 and 23 (32.4%) patients had BMIs greater than 35. Nine patients had diabetes (12.6%). Three patients (4.2%) had genetic mutations including 1 with BRCA1, 1 with BRCA2, and 1 with CHEK2 mutations. Fourteen
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(19.7%) patients had smoked within a year of surgery.
Sixty-eight (95.8%) patients elected to undergo contralateral reduction mammaplasty at
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the time of partial mastectomy to achieve symmetry. One patient had previous contralateral breast cancers treated with mastectomy and two patients declined contralateral symmetry procedure. Six (8.5%) patients underwent neoareolar reductions for central cancers that abutted or involved the nipple areolar complex. Average specimen weight was 415 ± 259.9g for the
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cancer side and 367 ± 240.7 for the contralateral side.
The average disease span was 31.4 mm (range 3-166 mm). No tumor on ink was achieved in 68 (95.8%) patients, all three positive margins were for DCIS. No tumor on ink but
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inadequate margins for DCIS, defined as <2mm, occurred in 3 (4.2%) patients. Four patients
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(5.6%) underwent re-excision for inadequate margins and had no residual invasive carcinoma or DCIS on their re-excision pathology. Two patients (2.8%) underwent mastectomy; one of them had 65mm of residual DCIS and the other had 110mm of residual IDCA and DCIS on final pathology.
Twenty (28.2%) patients received systemic chemotherapy. Thirteen (18.3%) patients underwent adjuvant chemotherapy and 7 (9.9%) patients underwent neoadjuvant chemotherapy. Radiation therapy was recommended for 67 patients; twenty-one (29.6%) patients elected to
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participate in the IORT protocol at the time of partial mastectomy. Five of those 21 (23.8%) patients were found to have higher risk disease requiring additional whole breast external beam radiation therapy. Forty-two (59.2%) patients elected to undergo standard external beam
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radiation. Four (6.0%) patients declined adjuvant whole breast radiation therapy, with 2 IORT patients electing for no additional radiation despite presence of high risk features. Fifty three of the fifty-six patients advised to take adjuvant endocrine therapy were started on endocrine
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therapy.
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No patients had major perioperative complications including pulmonary embolism, myocardial infarction, or cerebrovascular accident. No patients required extended hospital stay and none was readmitted to the hospital for complications. Twenty-three (32.4%) patients were reported to have surgical site complications including 13 patients who experienced complications on the cancer-side, 2 who experienced complications on the contralateral side, and 8 who
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experienced bilateral surgical site complications (Table 3). Triple point ulceration, a superficial epidermal separation at junction of the vertical incision and inframammary incision of the wisepattern breast reduction, occurred in 18 (25%) patients. None of the 6 patients who required
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complications.
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central partial mastectomy and reconstruction with neoareolar reduction experienced
Eleven (15.4%) patients required interventions. Sixteen patients (22.5%) experienced
Clavien-Dindo I complications with 4 requiring outpatient wound care. Three patients (4.2%) experienced Clavien-Dindo II complications and required outpatient antibiotics for presumed wound infections. Four patients (5.6%) experienced Clavien-Dindo III complications. One patient required scar revision under local anesthesia and one underwent a core needle biopsy
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(Clavien-Dindo IIIa), and two patients required scar revision under general anesthesia (ClavienDindo IIIb). No Clavien-Dindo IV complications were observed.
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Smoking status, BMI, whole breast radiation, and presence of diabetes were not associated with an increased rate of complications on both univariate and multivariate analyses. Intraoperative radiation was associated with a higher rate of complications (52.3% vs 20.3%, p=0.003) on univariate analysis. Larger specimen weight was also associated with a higher rate
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of complications on univariate analysis, with an average specimen weight of 514.1g in the
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complications group compared to 355.9g in patients without complications (p= 0.002). IORT was the only variable to reach significance on multivariate analysis (p=0.04); however, the rate of interventions for complications was not statistically different for complications associated IORT (45.5% vs 30%, p=0.45). Two of the four Clavien-Dindo III complications occurred in
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patients who received IORT.
Cosmesis was assessed post-operatively and reported in 67 (94.3%) patients (Table 4). Of the patients that had cosmetic scores, 64 (95.5% of those with reported scores and 90.1% of
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all patients) achieved good or excellent scores. Only 3 (4.5% of those with reported scores, 4.2% of all patients) patients had fair or poor cosmetic outcomes. Twenty-two (95.7%) of the 23
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patients who experienced complications had cosmetic scores reported. Twenty (90.1%) patients had good or excellent cosmetic outcomes. One patient had a fair outcome and one had a poor cosmetic outcome. All four patients who required re-excision achieved excellent cosmetic outcomes.
The average follow for this study was 32.1 months (range 6-54 months). There was one recurrence at 8 months during the follow-up interval. Three (4.2%) patients died during the
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follow-interval, all unrelated to breast cancer. One patient died from metastatic endometrial cancer, one from acute myelogenous leukemia, and one from heart failure.
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DISCUSSION Overall, the oncologic outcomes associated with oncoplastic reduction mammaplasty were excellent. Rate of inadequate margins (9.8%) and need for mastectomy (2.8%) were low
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and consistent with recent studies despite having relatively large tumors (average 31.4 mm, ranging up to 166 mm).18 Inadequate margins were all for DCIS, the full extent of which is
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notoriously challenging to ascertain on preoperative imaging.20 The patients who underwent reexcision had benign tissue on re-excision pathology and the two patients who underwent mastectomy had significant residual disease that was resected at the time of mastectomy. Adherence to adjuvant therapy recommendations was high and consistent with all
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patients undergoing breast cancer treatment at our institution. Recurrence rate was low with only 1 patient experiencing a recurrence during the follow up interval. Together, these findings suggest that reduction mammaplasty has excellent oncologic outcomes and may help patients to
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avoid mastectomy.
Oncoplastic reduction mammaplasty performed by surgical breast oncologists was
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associated with a low rate of surgical site complications. Thirty-two percent of patients in our study experienced minor wound complications and required few interventions or revisions. Clavien-Dindo III complications were rare and only occurred in 5.6% of patients. No ClavienDindo IV complications were observed. Even though we did not exclude patients at high risk for complications, our complication rate remained similar to that quoted in the plastic surgery literature, which ranges from 4-63%
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for reduction mammaplasties performed for symptomatic macromastia.21-30 Rates of surgical site complications associated with reduction mammaplasty are similar regardless of whether it is performed for symptomatic macromastia or in the treatment of breast cancer.31 According to the
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plastic surgery literature, risk factors for complications with reduction mammaplasty include higher BMI, increased specimen weight, smoking history, as well as use of intraoperative radiation therapy.6,21-33
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Patients in our study were offered oncoplastic reduction mammaplasty regardless of BMI, smoking status, age, and presence of diabetes. Our study found than none of these factors was
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associated with an increased rate of surgical site complications. This finding was consistent with previous studies that we have performed at our institution.32 As a result, we contend that oncoplastic reduction mammaplasty may be safely offered to patients with elevated BMI, advanced patient age, and presence of diabetes and recent smoking history. All patients should
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be counseled regarding potential risks associated with these factors; however in the setting of cancer, oncoplastic reduction mammaplasty remains an option. Factors associated with increased rate of complications on univariate analysis included
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larger specimen weight as well as IORT. IORT was the only factor that was associated with an
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increased rate of complications on multivariate analysis. Complications occurred in eleven (52.4%) patients who underwent IORT but the rate of interventions was not statistically different compared to complications that occurred in patients that were not exposed to IORT. Additionally, complications associated with IORT were minor, which was consistent with previous studies at our institution.32 As a result, we counsel patients appropriately prior to treatment and offer IORT to all patients who meet inclusion criteria for the institutional IORT study.
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Silverstein et al suggest that patients who complete BCT in a single operation have improved quality of life, improved cosmesis, less pain, and reduced health care costs compared to patients who require multiple operations.18 The majority of patients in our study were able to
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complete their BCT in one operation and achieved favorable cosmetic outcomes with over 90% of patients achieving good or excellent outcomes. Cosmetic outcomes remained favorable even when patients required re-excision or experienced complications.
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A multidisciplinary approach is the standard model for advanced oncoplastic surgery
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techniques, including reduction mammaplasty. Although the multidisciplinary surgery model can produce outstanding oncologic and cosmetic outcomes, it can present challenges with localization of the tumor bed and margins that require re-excision when inadequate margins are found on final pathology since the tissue rearrangement by the plastic surgeon may alter the location of margins. Additionally, scheduling can often be more complex when multiple
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surgeons are required for a case and may discourage patients from pursuing oncoplastic surgery. Unlike other studies, patients in this series underwent reduction mammaplasty performed
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exclusively by surgical breast oncologists without the assistance of plastic surgeons. When reexcision was required, accurate localization could be done since the surgeon who performed the
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cancer resection also performed the oncoplastic closure. All patients who had re-excision had their prior partial mastectomy sites confirmed by intraoperative identification of the surgical clips that had been placed to mark the resection margins at the time of their index operation. Intraoperative sterile inking along with meticulously mapped pathology also aided in the accurate localization of the tumor bed. Cosmesis was not compromised by re-excision, as all 4 patients who underwent re-excision achieved excellent cosmesis.
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One of the limitations to this study is that it is a retrospective single institution study that evaluates the outcomes of a limited number of patients who were operated on by two surgical breast oncologists with special training in oncoplastic surgery. Additionally, our pathology
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department is able to give us gross evaluation of margins as well as detailed maps of surgical specimens with the final pathology report which significantly improves our ability to address inadequate margins. Some institutions may not have the pathology resources to be able to
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provide this level of detail for both intraoperative and postoperative assessment and localization
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of inadequate margins. These factors may reduce the generalizability of our study. CONCLUSIONS
Oncoplastic reduction mammaplasty has expanded the indications for BCT.7-9 This study demonstrates that oncoplastic reduction mammaplasty can be performed safely by appropriately-
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trained surgical breast oncologists with an acceptable complication profile and achieve excellent oncologic and cosmetic outcomes.
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Cosmesis Grading
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EXCELLENT: when compared to the untreated breast or the original appearance of the breast, there is minimal or no difference in the size or shape of the treated breast. The way the breast feels (its texture) is the same or slightly different. There may be thickening, scar tissue or fluid accumulation within the breast, but not enough to change the appearance. GOOD: there is a slight difference in the size or shape of the treated breast as compared to the opposite breast or the original appearance of the treated breast. There may be some mild reddening or darkening of the breast. The thickening or scar tissue within the breast causes only a mild change in the shape or size. FAIR: obvious differences in the size and shape of the treated breast. This change involves a quarter or less of the breast. There can be moderate thickening or scar tissue of the skin and the breast, and there may be obvious color changes. POOR: marked change in the appearance of the treated breast involving more than a quarter of the breast tissue. The skin changes may be obvious and detract from the appearance of the breast. Severe scarring and thickening of the breast, which clearly alters the appearance of the breast may be found.
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Table 1. Cosmesis Scale.
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Patients n=71 Patient Characteristics Age (years) BMI (kg/m2) Smoking History Diabetes Genetic Mutation BRCA 1 BRCA 2 CHEK2
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Tumor Characteristics Size (mm) Side Left Right Histology Invasive Ductal Carcinoma Invasive Lobular Carcinoma Invasive Carcinoma with Ductal and Lobular Features Ductal Carcinoma-in-situ Other Grade Grade 1 Grade 2 Grade 3 Unknown Focality Unifocal Multi-focal Multi-centric Receptor Status ER positive PR positive Her2 positive
Surgery Characteristics Specimen Weight (g) Cancer Side Contralateral Side Bilateral Reduction Neoareolar Reduction
19.7% 12.7% 4.2% 1.4% 1.4% 1.4%
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59.6±10.8 31.9±5.4 14 9 3 1 1 1
%
42 29
59.2% 40.8%
43 6 6 12 4
60.6% 8.5% 8.5% 16.9% 5.6%
16 27 26 2
22.5% 38.0% 36.6% 2.8%
59 8 4
83.1% 11.3% 5.6%
60 42 7
84.5% 59.2% 9.9%
415±259.9 367±240.7 68 6
95.8% 8.5%
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No tumor on ink <2mm margins for DCIS Re-excision Mastectomy
68 3 4 2
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Adjuvant Therapies Chemotherapy Neoadjuvant Chemotherapy Adjuvant Chemotherapy Radiation Therapy IORT Whole Breast Both IORT and Whole Breast* Endocrine Therapy**
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20 7 13 63 21 47 5 53
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Table 2. Patient, tumor, and surgery characteristics.
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95.8% 4.2% 5.6% 2.8%
28.2% 9.9% 18.3% 88.7% 29.6% 66.2% 7.0% 74.6%
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%
31 (in 23 patients) 18 1 2 1 7 2
22.3% 12.9% 0.7% 1.4% 0.7% 5.0% 1.4%
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Interventions Total Wound care Scar revision Antibiotics Core Needle Biopsy
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Table 3. Complications and interventions.
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25 2 4 0
11 4 3 3 1
0.0% 18.0% 1.4% 2.9% 0.0%
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Clavien-Dindo Grade Clavien-Dindo I Clavien-Dindo II Clavien-Dindo III Clavien-Dindo IV
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Complications Total Triple point ulceration Seroma Hematoma Nipple Necrosis Fat Necrosis Infection
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Number of breasts n= 139
7.9% 2.9% 2.2% 2.2% 0.7%
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n = 23 13 7 1 1 1
63.4 26.8 2.8 1.4 5.6
56.5 30.4 4.3 4.3 4.3
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Patients with complications excellent good fair poor unknown
%
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All patients excellent good fair poor unknown
number of patients n = 71 45 19 2 1 4
Table 4. Cosmetic Outcomes at 6 months post-operatively.
[FIGURE 1 is uploaded separately as a PDF]
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Figure 1. Pre-operative (a) and post-operative (b) appearance of wise-pattern reduction mammaplasty incisions and surgical scars.
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30. Gust MJ, Smetona JT, Persing JS, et al. The impact of body mass index on reduction mammaplasty. Aesthetic Surg J. 2013;33:1140–1147. 31. Gulcelik MA, Dogan L, Camlibel M et al. Early Complications of a Reduction Mammaplasty Technique in the Treatment of Macromastia With or Without Breast Cancer. Clinical Breast Cancer. 2011; 11(6): 395-399.
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32. Crown A and Grumley JW. Association of Intraoperative Radiotherapy in the Treatment of Early-Stage Breast Cancer With Minor Surgical Site Complications in Oncoplastic BreastConserving Surgery. JAMA Surg. 2017. Epub ahead of print. 33. Manahan MA, Buretta KJ, Chang D et al. An outcomes analysis of 2124 breast reduction procedures. Ann Plast Surg. 2015. 74(3):289-92.
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34. Regano S, Hernanz F, Ortega E et al. Oncoplastic techniques extend breast-conserving surgery to patients with neoadjuvant chemotherapy response unfit for conventional techniques. World J Surg. 2009;33:2082-2086.
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Oncoplastic surgery expands the indications for breast conservation
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Oncoplastic surgery can be offered to patients despite presence of comorbidities
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Reduction mammaplasty has excellent cosmetic and oncologic outcomes
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Surgical breast oncologists can effectively perform reduction mammaplasties
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The authors have no conflicts of interest.