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Recommendations for Pathologic Evaluation of Reduction Mammoplasty Specimens: A Prospective Study With Systematic Tissue Sampling.

Reduction mammaplasty (RMP) is a very common surgical procedure. In their 2015 procedural statistics, the American Society of Plastic Surgeons reported 106 338 breast reconstructive procedures performed in the United States. (1) Bilateral breast reduction is most commonly performed for symptomatic macromastia, and unilateral breast reduction (balancing) is frequently used to improve asymmetry due to cancer surgery or congenital causes.

Although surgeons routinely submit breast RMP specimens for pathologic assessment, no standardized pathology procedure for processing and examination of these specimens exists. RMP specimens routinely arrive in surgical pathology fragmented because of the nature of the surgical procedure. The fragmentation and inability to assess margin status contributes to the absence of a standardized assessment. Following gross evaluation of RMP specimens, the number of tissue sections submitted for histologic/microscopic assessment varies from institution to institution. The incidence of clinically occult breast cancer in RMP specimens is reported to range from 0.06% to as high as 12.8%. (2-30)

Goodwin et al (31) previously reported a retrospective 5-year study of 552 RMP cases and demonstrated a carcinoma rate of 0.9%. In addition, they identified 5 cases (0.9%) of atypical hyperplasia. Their institutional pathologic assessment consisted of gross examination followed by microscopic examination of 3 sections of breast tissue and 1 section of skin. In this retrospective study, the mean age of patients with carcinoma or atypical hyperplasia was statistically significantly higher compared with women without carcinoma or atypia.

During the time of this study, the American Cancer Society recommended routine mammography screening for women starting at age 40. (32) The current American Cancer Society recommendation is for routine annual mammography screening for women at average risk starting at age 45 years, with an opportunity to start between ages 40 and 44 years given the increased incidence of breast cancer in these age groups compared with the younger population. (33) Similarly, guidelines for pathologic assessment for RMP specimens should be developed, particularly for women older than 40 years and those with an increased risk of breast cancer because of family or personal history.

The primary objective of this prospective study was to evaluate the effect of different sampling strategies for RMP specimens and to use the data to propose evaluation guidelines for pathology. Additional objectives included determining the incidence of significant pathologic findings (SPF), defined as occult carcinoma and atypical hyperplasia (including atypical ductal hyperplasia [ADH] and atypical lobular hyperplasia [ALH]), in RMP specimens. Associations between pathologic findings and age, specimen weight, proliferative and nonproliferative lesions, microcalcifications, and other predictive clinical risk factors were investigated. Lastly, systematic sequential sampling of additional tissue sections was used to evaluate whether increased sampling would identify additional SPF.

MATERIALS AND METHODS

This study was approved by the University of Vermont (Burlington) Institutional Review Board for protection of human subjects in research.

Following a baseline retrospective study, we began a prospective study of all RMP cases in our institution. All consecutive RMP cases from 2006 to 2013 were included in this study. Gross pathology evaluation was performed by board-certified pathologist assistants (PAs). Five pathology assistants have participated during this study. The first PA performed a gross examination of the specimen and selected 3 sections of breast tissue and 1 section of skin for microscopic evaluation. These were submitted in 2 tissue cassettes and defined as tissue section set (TSS) 1. This was also the standard baseline assessment for RMP specimens in our institution prior to initiating this study. For the purpose of this study, additional breast tissue sections were systematically evaluated. A second PA performed an additional gross evaluation and submitted 8 additional sections for microscopic evaluation in 4 tissue cassettes. The second PA was instructed to rank order the submitted sections, with the most suspicious or fibrous areas placed into TSS-2 (4 sections of breast tissue) and additional fibrous tissue submitted in TSS-3 (4 sections of breast tissue). The PA staff rotated responsibility as the first or second PA on a weekly basis. The combined sampling resulted in 11 total breast sections and 1 skin section for histologic examination from each breast.

Paraffin-embedded, hematoxylin-eosin-stained slides were prospectively reviewed by 4 breast pathologists in our institution (A.A., A.G., T.S., and D.W.) and detailed findings recorded on a data form. The form included surgical pathology number, weight of the specimen, and a detailed checklist of pathologic findings and their location in the tissue blocks and TSSs. Data from the form were transferred to a database that also recorded patient age, history of contralateral breast cancer, interval between preoperative mammogram and surgery, follow-up management, and operating surgeon. Significant pathologic findings were defined as invasive carcinoma, ductal carcinoma in situ, lobular carcinoma in situ, ADH, or ALH. Although data from each tissue set were analyzed separately for research purposes, the final diagnosis reported to the surgeon for clinical management represented the pathologic findings from the entirety of the submitted tissue.

The association between age and SPF was calculated using Fisher exact test and t test (SAS v 9.4, SAS Institute Inc, Cary, North Carolina). Exact binomial confidence intervals are reported.

Following the recommendation of American Cancer Society breast screening guidelines during the study period and standard practices in our institution, all patients aged 40 years or older had screening mammography within 1 year preceding RMP surgery. There were no patients whose RMP surgery was deferred or cancelled because of an abnormal preoperative screening mammogram.

Review of electronic medical records was undertaken after 34 to 126 months follow-up.

RESULTS

A total of 595 patients were evaluated during the study period. There were 518 procedures (87%) for macromastia (Figure 1, A and B) and 77 procedures (13%) for balancing because of contralateral breast cancer. All breast tissue and skin specimens were received as many fragmented pieces (Figure 1, C). The mean age of all patients was 44.6 years; the median age was 46 years (range, 14-82 years). The median weight of RMP specimens was 514 g and the mean weight was 572.7 g (range, 5.4-2460 g). Significant pathologic findings were identified in 9.8% (58 of 595; 95% CI, 7.5%-12.4%) of all patients (Table 1). Carcinoma was present in 2.4% (14 of 595; 95% CI, 1.3%-3.9%) of all patients, including 2 invasive carcinomas, 6 ductal carcinomas in situ, and 6 lobular carcinomas in situ. One of the 6 lobular carcinoma in situ cases was pleomorphic type (Figure 1, D through F). The average size of the carcinomas was 4.3 mm (range, 2-18 mm). The 2 invasive carcinomas were well differentiated, ductal type, not otherwise specified (NOS), and measured 4.0 and 5.0 mm under the microscope. The largest ductal carcinoma in situ (18.0 mm) was a noncalcifying tumor with intermediate nuclear grade and no necrosis. Carcinomas were identified only in patients 40 years or older (14 of 392; 3.6%).

In this series, 65.9% (392 of 595) of all patients were 40 years of age or older. Overall, there were 58 incidences of SPF (Table 1). Age was significantly associated with SPF in the analysis of pathologic findings from all 3 tissue sets combined (P < .001; Table 1). Mean ages were 51.7 and 42.9 years in patients with and without SPF, respectively. The majority of the patients with SPF (54 of 58; 93.1%) were older than 40 years (Fisher exact test P = .002; Figure 2). The 4 remaining patients with SPF were 35, 38, 38 and 39 years old. Two of these patients had unilateral disease (both ALH) and 2 had bilateral disease: 1 had ALH in both breasts, and 1 had ALH in one breast and ADH in the other (Table 2). In the group of patients older than 40 years, the rate of SPF was 13.8% (54 of 392), and the rate of carcinoma was 3.6% (14 of 392; 95% CI, 2.7%-11.8%). The highest rate of SPF was found in patients 50 years of age or older (15.9%; 37 of 233). In this age group, the rate of carcinoma was 4.3% (10 of 233; 95% CI, 2.9%-16.4%). No carcinoma was identified in patients younger than 40 years. No SPF were identified in patients younger than 35 years.

Increased sampling was associated with a significantly greater frequency of SPF (Table 3). Although 43.1% of SPF (25 of 58) were identified in TSS-1, both TSS-1 and TSS-2 together identified 82.8% of all SPF (48 of 58). An additional 17.2% of SPF (10 of 58) were identified in TSS-3 (Table 3). Increased sampling was significantly associated with increased SPF only in patients aged 40 years or older (P = .02). In patients younger than 40 years, increased sampling did not lead to significant increase in SPF (P = .20). Patients with carcinomas were also significantly older than patients without carcinomas (52.9 versus 44.4, t test P =.04).

The majority of patients (87%) had undergone bilateral RMP for macromastia. There were 77 patients with a history of contralateral breast cancer who had undergone surgery to improve symmetry. The rate of SPF in the 77 patients with a history of contralateral breast cancer undergoing surgery to improve symmetry was 16.9% (13 of 77), which was higher than in patients without history of breast cancer (8.7%; 45 of 518). However, when adjusted for age, a history of contralateral breast cancer was not a significant predictor for SPF (P = .48).

Sixty-one patients (10.3%) with a mean age of 49.3 years (range, 16-76 years) were found to have skin lesions on microscopic histologic examination. All skin lesions were first identified clinically and/or during gross examination. The majority of lesions were seborrheic keratosis (34 of 61; 55.7%), followed by melanocytic nevi (15 of 61; 24.6%) and capillary hemangiomas (8 of 65; 13.1%). There were 2 patients with epidermal inclusion cysts and 1 patient each with acantholytic acanthoma and multiple lentigines.

The length and size of this study allowed for long-term follow-up of RMP patients. The electronic medical record review of only the patients that underwent RMP for macromastia (518 of 595) ranged from 34 to 126 months. There was a significantly higher rate of subsequent recurrent SPF in patients who showed SPF in their original RMP (8.9%; 4 of 45) than in patients with no SPF in their RMP procedure (0.4%; 2 of 473; 95% CI, 2.5%-21.2%; Fisher exact test P < .001). It should, however, be noted that patients with a history of SPF in their original RMP were placed in a high-risk patient category and had more frequent follow-ups than patients without SPF in their original RMP. These patients were also offered prophylactic hormonal treatment.

DISCUSSION

This prospective study used systematic pathologic tissue evaluation of RMP specimens in patients with and without history of breast cancer. Our prospective series of women undergoing RMP demonstrated a high rate of SPF (9.8%). There was a 2.4% prevalence of carcinoma in the entire group. The prevalence of carcinoma was 3.6% in women 40 years of age or older and 4.3% in patients 50 years or older. These findings impact a large group of women when extrapolated to the more than 100 000 RMP procedures performed each year in the United States. (1) The 9.8% rate of SPF translates to approximately 10 000 patients annually who would potentially benefit from altered clinical management. More than 2400 patients could potentially be diagnosed with invasive or in situ carcinomas based on the 2.4% overall carcinoma rate in our data.

In the women undergoing balancing RMP procedure for contralateral breast cancer, the rate of SPF was 16.9%, which was higher than the 8.7% in patients without history of breast cancer. However, when adjusted for age, a history of contralateral breast cancer was not a significant predictor for SPF.

In our institution, each patient with SPF is surgically and medically managed based on the findings in the individual case. All patients with SPF are placed in a high-risk screening group with close clinical and imaging follow-up. In our series, patients with invasive and in situ carcinomas were treated similarly to other breast cancer patients in our comprehensive breast care center. However, these cases were complicated by the lack of standard margin assessment due to the fragmented nature of the RMP specimens (Figure 1, E).

Atypical hyperplasia (ADH and ALH) as an indicator of increased risk for developing breast cancer is well established, with reported relative risk ranging from 4% to 6%. (34-36) Hence, in our institution, patients with a diagnosis of atypical hyperplasia were offered prophylactic hormonal treatment and/or high-risk follow-up.

The majority of patients with SPF underwent screening mammogram within the year prior to RMP, with most patients having undergone screening within 6 months prior to surgery. However, none of the pathologic findings were detected on preoperative screening mammogram. This suggests that additional preoperative screening mammograms as recommended by other authors are unlikely to have added benefit in RMP patients. (10,37,38) Although some studies have shown MRI to be more sensitive than mammography in detecting lesions in younger women, (39,40) particularly those with dense breasts or other risk factors, it would be difficult to justify screening MRI based on the cancer rates and size of the lesions detected in our series. Therefore, we follow American Cancer Society screening guidelines for women 40 years and older. (33) For women younger than 40 years, breast screening prior to RMP can be tailored to risk, based on the patient's family history. We also recommend that patients undergoing RMP surgery be informed of the small possibility of occult breast cancer diagnosis.

The invasive carcinomas and the majority of the in situ carcinomas identified in this study were small, non-massforming, noncalcifying lesions; hence, they were not detected on preoperative screening mammograms or on gross pathologic examination. All were identified incidentally on microscopic examination only.

All pathologic skin findings were evident on clinical and/or on gross pathologic examination. This indicates that random sampling of skin for microscopic examination is unnecessary in the absence of clinically and/or visually apparent lesions.

Our study demonstrated that identification of SPF is significantly associated with increased sampling of RMP specimens. However, there was a break point at age 40, below which the association was no longer statistically significant (Figure 2). Our findings suggest that in women younger than 40 years, a thorough gross examination and limited histologic evaluation may be adequate. Furthermore, no SPF were identified in women younger than 35 years, suggesting microscopic evaluation may not be necessary unless there are abnormal findings on thorough gross examination or the patient has a strong family history or genetic abnormalities. Bondeson et al (41) reviewed 200 RMP specimens in which the majority of patients were 30 years of age and younger and found no SPF. They suggested that thorough gross examination without microscopic examination may be adequate in patients younger than 30 years. Although this was not specifically evaluated in our study, we believe that a family history of breast cancer should be considered when evaluating RMP specimens from younger women. Thorough microscopic evaluation should be undertaken in women with a known carrier mutation such as BRCA-1 or BRCA-2. In addition, when a positive family history is given by the submitting surgeon, thorough sampling is prudent for RMP specimens beginning at an age 10 years younger than that of the youngest direct relative with breast cancer.

The patient population in our study consisted mainly of white patients, with a low number of African American women, who may have higher risk for breast cancer at younger age. (42)

On follow-up review of electronic medical records, there were significantly more recurrences in patients who had SPF in their RMP (8.9%; 4 of 45) than patients without SPF (0.4%; 2 of 473). This may partially be explained by the fact that patients with a history of SPF were placed in a high-risk patient category and had more frequent clinical and radiographic follow-up than patients without SPF.

No standardized procedure for processing and examination of RMP specimens exists in the pathology literature. Our study revealed that more histologic sampling of RMP specimens leads to significantly increased identification of occult SPF in women older than 40 years. These associations were not seen in patients younger than 40 years. Based on the data from this prospective study, we propose a tiered sampling strategy of RMP specimens based on patient age and personal or family history. Hence, we recommend the following tissue-section-sampling scenarios for RMP specimens:

1. In patients younger than 35 years: Thorough gross evaluation with sampling for microscopic evaluation only when suspicious lesions are identified or there is a strong family history of breast cancer, that is, breast cancer in first-degree relatives.

2. In patients 35 to 49 years old: 6 to 7 breast sections.

3. In patients 50 years or older: 10 to 11 breast sections.

4. In patients undergoing balancing RMP: Based on our study, no special consideration may be required based on a history of contralateral breast cancer (it should be based only on patient age).

5. Skin sampling for microscopic evaluation is not required unless there is a clinically and/or grossly identified skin lesion.

The above sectioning scenario would target and identify the vast majority of patients who are likely to have carcinoma and/or atypical hyperplasia(s) in RMP specimens. However, there will be an overall increase in the number of tissue blocks submitted, on average an increase by 1 tissue block per breast (ie, 3 tissue blocks, compared with the baseline uniform 2 tissue blocks for each breast used in our institution prior to the current study).

The authors thank the following pathology assistants: Amanda Duckworth, MS; Laura Fleming, MS; Michelle C. Schwartz, MS; Jayne D. Tessitore, MS; and Joseph J. Tessitore, MS.

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Abiy B. Ambaye, MD; Andrew J. Goodwin, MD; Susan E. MacLennan, MD; Shelly Naud, PhD; Donald L. Weaver, MD

Accepted for publication February 15, 2017.

Published as an Early Online Release August 10, 2017.

From the Departments of Pathology and Laboratory Medicine (Drs Ambaye, Goodwin, and Weaver) and Surgery (Dr MacLennan), University of Vermont Medical Center, Burlington; and the Department of Medical Biostatistics, University of Vermont, Burlington (Dr Naud).

The authors have no relevant financial interest in the products or companies described in this article.

Funding for Dr Naud's statistical analyses was provided by the Lake Champlain Cancer Research Organization (LCCRO).

Presented in part at the 105th annual meeting of the United States and Canadian Academy of Pathology;March 21-27, 2015; Boston, Massachusetts.

Reprints: Abiy B. Ambaye, MD, Department of Pathology and Laboratory Medicine, University of Vermont Medical Center, ACC EP2, 152, 111 Colchester Ave, Burlington, VT 05401 (email: Abiy.B. Ambaye@uvmhealth.org).

Please Note: Illustration(s) are not available due to copyright restrictions

Caption: Figure 1. A, Macromastia, before reduction mammaplasty (RMP) surgery. B, Post-RMP surgery. C, RMP specimen, gross. D, Ductal carcinoma in situ. E, Pleomorphic lobular carcinoma in situ. F, Invasive carcinoma (hematoxylin-eosin, original magnifications X40 [D], X100 [E], and 320 [F]).

Caption: Figure 2. Age distributions of patients with carcinoma, atypical ductal hyperplasia (ADH), and atypical lobular hyperplasia (ALH).
Table 1. All Reduction Mammoplasty Patients

Patients            All        No SPF     With SPF     P
                 (N = 595)   (n = 537;    (n = 58;
                             90.2%) (a)    9.8%)

Specimen type,                                       <.001
No.
Reduction        518 (87%)      473          45
Balancing (b)    77 (13%)        64          13

Age y                                                <.001
Range              14-82       14-82       35-71
Mean               44.6         42.9        51.7
Median              46           46          51

Average breast                                        .16
weight, g
Right              569.8       562.6       532.2
Left               575.6       551.8       550.4
Total              572.7       557.2       541.3

Abbreviation: SPF, significant pathologic findings.

(a) Significant pathologic findings include atypical ductal
hyperplasia, atypical lobular hyperplasia, lobular carcinoma
in situ, ductal carcinoma in situ, and invasive carcinoma.

(b) Patients with a history of breast cancer undergoing
reduction mammaplasty surgery for symmetry.

Table 2. Significant Pathologic Findings According to Diagnosis

Age y             Benign, No.   ALH,    LCIS,   ADH,    DCIS,
                      (%)        No.     No.     No.     No.

[greater than     338 (82.2)     29       6      11       6
or equal to] 40
<40                199 (98)     3 (a)     0     1 (a)     0
Total             537 (90.3)     32       6      12       6

Age y             Invasive,   Total, No.
                     No.         (%)

[greater than         2       392 (65.9)
or equal to] 40
<40                   0       203 (34.1)
Total                 2          595

Abbreviations: ADH, atypical ductal hyperplasia;ALH, atypical
lobular hyperplasia;DCIS, ductal carcinoma in situ; LCIS, lobular
carcinoma in situ.

(a) These 4 patients were 35, 38, 38, and 39 years old.

Table 3. Significant Findings According to Tissue
Section Set (TSS)

                     TSS-1,       TSS-2,       TSS-3,
Diagnosis           No. (a)      No. (b)      No. (c)

ALH (n = 32)           11           13         8 (d)
LCIS (n = 6)           5            1            ...
ADH (n = 12)           6            4          2 (e)
DCIS (n = 6)           3            3            ...
Invasive (n = 2)       ...            2          ...
Total (n = 58)     25 (43.1%)   23 (39.7%)   10 (17.2%)

Abbreviations: ADH, atypical ductal hyperplasia; ALH,
atypical lobular hyperplasia;DCIS, ductal carcinoma in
situ; LCIS, lobular carcinoma in situ.

(a) Diagnosis made first on TSS-1 regardless of findings
in TSS-2 and/or TSS-3.

(b) Diagnosis made first on TSS-2, regardless of findings
in TSS-3.

(c) Diagnosis made solely on TSS-3.

(d) Patient ages were 38, 40, 41 (2), 49, 54, 55, and
68 years.

(e) Patient ages were 56 and 57 years.
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Author:Ambaye, Abiy B.; Goodwin, Andrew J.; MacLennan, Susan E.; Naud, Shelly; Weaver, Donald L.
Publication:Archives of Pathology & Laboratory Medicine
Article Type:Report
Geographic Code:1USA
Date:Nov 1, 2017
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