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Available online at www.sciencedirect.com

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Malignancy rates after surgical excision of discordant breast biopsies Barish B. Poole, BA,a Julie S. Wecsler, MD,b Pulin Sheth, MD,c Stephen F. Sener, MD,b Lina Wang, MD,d Linda Larsen, MD,c Debu Tripathy, MD,e and Julie E. Lang, MDb,* a

Keck School of Medicine, University of Southern California (USC), Los Angeles, California Department of Surgery, Section of Breast and Soft Tissue Surgery, USC Norris Comprehensive Cancer Center, Los Angeles, California c Department of Radiology, Division of Breast Imaging, USC Norris Comprehensive Cancer Center, Los Angeles, California d Department of Pathology, Keck Hospital of USC, Los Angeles, California e Department of Medicine, Division of Medical Oncology, USC Norris Comprehensive Cancer Center, Los Angeles, California b

article info

abstract

Article history:

Background: Vacuum-assisted core-needle biopsy (VAB) is increasingly used to perform

Received 27 September 2014

breast biopsies instead of automated-gun core-needle biopsy (CNB). The significance of

Received in revised form

discordance between radiologic and pathologic findings has not been well established in the

19 November 2014

era of VAB predominance. This retrospective study was conducted to determine the rate of

Accepted 21 November 2014

malignancy after surgical excisional biopsy (EXB) of these lesions at our two institutions.

Available online 27 November 2014

Materials and methods: We reviewed medical records from January 2008eJune 2013 to identify female patients who underwent EXB for a Breast Imaging-Reporting and Data

Keywords:

System (BI-RADS) 4 or 5 lesions found to be benign and discordant on CNB. Clinicopatho-

Breast cancer

logic data were gathered, and analysis was performed using descriptive statistics.

Core-needle biopsy

Results: A total of 8081 core biopsies were performed in the study timeframe. Six of 81 (7.4%)

Breast surgery

patients who had an EXB for a benign discordant breast lesion were found to have ma-

Discordant

lignant pathology (two invasive, four in situ). Four of 63 (6.3%) lesions originally biopsied by

Benign breast

VAB were upgraded, compared with 2 of 17 (11.8%) originally biopsied by CNB. There were no statistically significant differences in the rates of upgrade to malignancy when data were stratified by BI-RADS score or method of biopsy. Conclusions: The overall rate of malignancy after EXB of benign discordant lesions was 7.4%. Despite the widespread adoption of VAB, EXB is still warranted for clarification of discordant radiologicepathologic findings. ª 2015 Elsevier Inc. All rights reserved.

1.

Introduction

Approximately 1.7 million breast biopsies are performed annually in the United States [1]. Percutaneous core-needle

breast biopsy is a rapid, accurate method of sampling radiologically or clinically suspicious breast lesions. It is useful in part for the identification of benign lesions that do not require excision [1e7]. Core-needle biopsy (CNB) has generally

* Corresponding author. Department of Surgery, Section of Breast and Soft Tissue Surgery, USC Norris Comprehensive Cancer Center, 1450 Biggy Street, Norris Research Tower (NRT) 3505, Los Angeles 90033, CA. Tel.: þ1 323 442 8140; fax: þ1 323 865 3539. E-mail address: [email protected] (J.E. Lang). 0022-4804/$ e see front matter ª 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jss.2014.11.032

j o u r n a l o f s u r g i c a l r e s e a r c h 1 9 5 ( 2 0 1 5 ) 1 5 2 e1 5 7

supplanted excisional breast biopsy (EXB) for sampling of image-detected lesions and is now considered the preferred method for initial diagnosis, having demonstrated accuracy essentially equivalent to EXB [1]. However, there is still potential for false-negative core-needle or EXB. Post-biopsy correlation of radiologic and pathologic findings is essential to correctly interpret pathology and avoid delay of malignant diagnoses [1,6,8e10]. Radiologicepathologic discordance, defined as suspicious radiographic findings not explained by pathology findings, raises suspicion of a false-negative benign core biopsy and the possible presence of a malignancy. This generally motivates the practice of following up discordant core biopsy results with EXB. The rate at which benign discordant lesions are upgraded to malignancy on EXB is not well characterized in the literature because of relatively few studies addressing this question. Reported percentages vary widely (0%e53.8%), and various interpretations have been made in regards to standard of care for obtaining a definitive diagnosis in these lesions [11e18]. Currently, the largest published study examining this rate for vacuum-assisted core-needle biopsies (VABs), which are increasingly used over the older automated-gun biopsy technology (CNB), is limited to the use of VAB in 20 patients [11]. VAB is reported to have reduced histologic underestimation, false negatives, and incidence of discordance, with a negative predictive value as high as 99.95% [12,19e25]. VAB has been the predominant method of biopsy at our two institutions for over 5 y, and we have continued to routinely perform EXB for discordant cases. We conducted this study to determine the rate of malignancy after EXB for benign discordant breast lesions worked up by a dedicated multidisciplinary breast oncology team in the contemporary era.

(MRI) guidance. Clips were placed and documented by mammography after biopsy for all patients. VAB devices used at LAC were as follows: 1) the Mammotome ST, EX, and elite systems (Mammotome, Cincinnati, OH); and 2) Hologic Celero and ATEC systems (Hologic Inc, Bedford, MA). CNBs were performed with the Bard Max-Core Disposable Core Biopsy Instrument (Bard, Murray Hill, NJ). VAB devices at Norris were as follows: 1) the Mammotome ST; 2) Hologic Eviva, Celero, and ATEC system; and 3) Bard EnCor and Vacora. After pathologic diagnosis of the tissue, a multidisciplinary team, including representative faculty from radiology, pathology, and breast surgical oncology, evaluated radiologicepathologic concordance. Figure describes the flow of patient workup that generated our study cohort of benign discordant lesions.

2.3.

Material and methods

2.1.

Patients

Post-biopsy management

Pathologically benign lesions considered discordant (radiographically suspicious despite a benign core biopsy) either underwent repeat CNB or were referred to surgery for removal by EXB, according to the radiologist’s recommendation and patient preference. In general, cases were reviewed again at our multidisciplinary conference before the scheduled surgery to confirm discordance. All patients managed by EXB were represented at the conference for review of surgical pathology and treatment planning. Our medical record database was not able to generate the number of patients with discordant pathology reports who did not have EXB during this time period; however, our standard operating procedure was to perform EXB for benign discordant lesions. Surgeries for Norris patients were performed at Keck Hospital of USC.

2.4.

2.

153

Data collection and statistical analysis

Charts of patients satisfying study criteria were reviewed for clinicopathologic variables including clinical presentation,

A retrospective review of medical records at both Los Angeles County Medical Center (LAC) and USC Norris Comprehensive Cancer Center (Norris) was performed to identify all female patients aged 18e90 y who had EXB of a benign discordant breast lesion from January 2008eJune 2013. Our radiologists’ practice is to provide a Breast Imaging-Reporting and Data System (BI-RADS) score for every abnormal imaged lesion as opposed to the whole breast. Only patients with BI-RADS 4 or 5 breast lesions were included in the study. Pathologic lymph nodes were not included, as this is a separate research question. Patients with any history of known malignancy were excluded. This study was approved by the University of Southern California Institutional Review Board.

2.2.

CNBs and radiologicepathologic correlation

All CNBs were performed by specialized radiologists or radiology residents under attending supervision. Biopsies at LAC varied between VAB and CNB at the discretion of the attending radiologist, whereas only VAB was performed for our patient cohort at Norris. Core biopsies were performed under ultrasound, stereotactic, or magnetic resonance imaging

Figure e Workflow for evaluation of breast findings. We retrospectively reviewed the medical records of 81 patients undergoing EXB for benign discordant CNB. Radiologicepathologic discordance was determined by a multidisciplinary team performing routine clinical breast examinations, screening, and diagnostic mammograms, and CNBs.

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imaging modalities, BI-RADS scores, CNB methods, number of repeat biopsies, pathologic findings, surgical complications, and postoperative treatment parameters. Distributions of categorical variables were tabulated, and rates of malignancy were calculated. Chi-square and Fisher exact tests were performed using GraphPad InStat (GraphPad Software Inc, San Diego, CA). Data were analyzed for all patients, as well as separately for patients from LAC and Norris.

3.

Results

3.1.

Patients

The annual number of screening mammograms performed at LAC in 2013 was 17,229, with 2088 called back for diagnostic mammography for a callback rate of 12.1%. The rate was similar at Norris, with 487 of 3852 (12.6%) screenings called back for additional views. A total of 8081 CNBs were performed during the study timeframe of January 2008eJune 2013d5919 at LAC and 2162 at Norris. These included repeat biopsies and biopsies for abnormalities that were first discovered by a method other than screening mammogram at one of our two institutions. Eighty-one female patients fit our inclusion criterion of receiving EXB for a BI-RADS 4 or 5 lesions associated with benign discordant pathologic findings. The median age was 51 y for 55 patients at LAC and was 46.5 y for 26 patients at Norris; this difference was not statistically significant (P ¼ 0.14). Clinicopathologic features of all cases and associated rates of malignancy after EXB are summarized in Table 1. Thirty-five of 81 (43.2%) patients presented with suspicious findings on screening mammography and 26 (32.1%) presented with a palpable mass. The remaining 20 (24.7%) patients presented with various other clinical indications, including nipple discharge or pain. Twenty of 81 (24.7%) lesions were BI-RADS 4A (low suspicion), 26 (32.1%) were BI-RADS 4B (intermediate suspicion), 26 (32.1%) were BI-RADS 4C (moderate suspicion), and 9 (11.1%) were BI-RADS 5 (highly suspicious).

3.2.

Core-needle biopsies

The 81 patients in our study underwent a total of 101 CNBs with discordant results, including repeat biopsies. This represents 74 of 5919 (1.3%) total biopsies at LAC and 27 of 2162 (1.2%) total biopsies at Norris performed during the study period. Eighteen of 55 (32.7%) LAC patients and 1 of 26 (3.8%) Norris patients underwent one or more repeat biopsies (Table 1). Of the 18 patients at LAC who received repeat biopsies, 12 (66.7%) had a VAB followed up with a second VAB, 2 (11.1%) switched from CNB to VAB, 1 (5.6%) followed a CNB with another CNB, and 3 (16.7%) switched from VAB to CNB. For each patient, procedural and pathologic data from only the last biopsy before EXB were included in our assessment. Of 54 lesions at LAC for which method of biopsy was identified, 37 (68.5%) biopsies were VAB and 17 (31.5%) were CNB. All biopsies done at Norris were VAB. The majority of all biopsies, both VAB and CNB, were ultrasound-guided (n ¼ 66, 82.5%). Nine (11.3%) biopsies were stereotactically guided, and 5 (6.3%) were MRIguided. At LAC, the majority of VABs were performed with 8-, 11-, or 12-gauge needles, whereas the majority of CNBs were performed with 14-gauge needles. MRI-guided biopsies were

Table 1 e Clinicopathologic features and malignancy rates of 81 benign discordant lesions. Lesion and biopsy characteristics

LAC Norris Malignant patients patients upgrade (n ¼ 55) (n ¼ 26) frequency (%)

BI-RADS category 4A 4B 4C 5 Clinical presentation Abnormal screening mammogram Palpable mass Nipple discharge Pain Suspected Paget disease Inflammation Other Histopathologic diagnosis on core biopsy Benign breast tissue Low risk (FCC, DHU, FA, FN) Intermediate risk (PPL, RS, SA, PASH) High risk (ALH, ADH, FEA) Other Insufficient sample with benign findings CNB method* Automated gun Vacuum-assisted Core-needle image guidance method* Ultrasound Stereotactic mammography MRI Core-needle gauge* 8 9 10 11 12 14 Repeat core biopsy performed Yes No

18 15 17 5

2 11 9 4

1/20 1/26 3/26 1/9

(5.0) (3.8)) (11.5) (11.1)

25

10

3/35 (8.6)

14 7 5 1 1 2

12 2 0 0 0 2

2/26 0/9 0/5 1/1 0/1 0/4

4 40

1 11

0/5 (0) 2/51 (3.9)

5

10

2/15 (13.3)

0 2 4

3 1 0

1/3 (33.3) 0/3 (0) 1/4 (25.0)

17 37

0 26

2/17 (11.8) 4/63 (6.3)

44 7

22 2

5/66 (7.6) 0/9 (0)

3

2

10 1 2 18 8 15

2 3 8 2 11 0

0/12 1/4 2/10 0/20 1/19 2/15

18 37

1 25

0/19 (0) 6/62 (9.7)

(7.7) (0) (0) (100.0) (0) (0)

1/5 (20.0) (0) (25.0) (20.0) (0) (5.3) (13.3)

ADH ¼ atypical ductal hyperplasia; ALH ¼ atypical lobular hyperplasia; DHU ¼ ductal hyperplasia of usual type; FA ¼ fibroadenoma; FEA ¼ flat epithelial atypia; FCC ¼ fibrocystic changes; FN ¼ fat necrosis; PASH ¼ pseudoangiomatous stromal hyperplasia; PPL ¼ papilloma; RS ¼ radial scar; SA ¼ sclerosing adenosis. * Biopsy technique not determined for n ¼ 1.

performed with 9- or 10-gauge needles. At Norris, 10- and 12gauge VAB needles predominated, although 8-, 9-, and 11-gauge needles were also used.

3.3.

Pathology

Preoperative histopathologic diagnoses are summarized in Table 1. After EXB, 6 of 81 (7.4%) patients were found to have

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malignant pathologyd3 of 55 (5.5%) at LAC and 3 of 26 (11.5%) at Norris. Five of 72 (6.9%) patients with a BI-RADS 4 lesion and 1 of 9 (11.1%) patients with a BI-RADS 5 lesion were upgraded to malignancy. Four of 63 (6.3%) lesions biopsied by VAB, and 2 of 17 (11.8%) biopsied by CNB were upgraded. None of the lesions that underwent repeat CNB were upgraded, whereas all six proven malignancies underwent only a single biopsy before EXB. Table 2 displays the clinicopathologic characteristics of the 6 malignant cases. Three were ductal carcinoma in situ (DCIS), 1 included both DCIS and lobular carcinoma in situ components, 1 was invasive ductal carcinoma with a DCIS component, and 1 was invasive lobular carcinoma. Of the 3 DCIS cases, CNB findings were consistent with fibrocystic changes in 1, fibroadenoma in 1, and papilloma with pseudoangiomatous stromal hyperplasia in 1, which had presented with a nipple rash suspicious for Paget’s disease. The DCIS/lobular carcinoma in situ case had been diagnosed on VAB as atypical lobular hyperplasia. The case upgraded to invasive ductal carcinoma was initially diagnosed as pseudoangiomatous stromal hyperplasia on VAB at Norris. The case of invasive lobular carcinoma was identified as fibrocystic changes on CNB at LAC, although it was noted by the pathologist that there was insufficient glandular tissue for diagnosis. The final benign diagnoses on surgical pathology for the other 75 lesions are summarized in Table 3. Fibrocystic changes (n ¼ 18, 24%) and fibroadenoma (n ¼ 16, 21.3%) predominated, with papilloma, sclerosing adenosis, and other benign lesions of varying risk comprising the remainder.

4.

Discussion

We found a rate of malignancy after surgical excision of 7.4% in a relatively large consecutive cohort of benign discordant breast lesions. Among studies including VAB and CNB, our overall rate falls near the low end of the range of frequencies (0%e53.8%) reported thus far [11e18]. Still, this false-negative rate specific to discordant CNBs is substantially higher than the false-negative rates reported in the literature for all VAB procedures, consistently found to be under 2% [12,19,26,27]. It

is more comparable with the rates reported for CNB, which can approach 10% [8,12,27,28]. Given that a benign-discordant VAB carried a risk of malignancy of 6.3% in our series, surgical EXB is warranted for these lesions. The malignancy upgrade rate at LAC (5.5%) was similar to that at Norris (11.5%; Table 1). The proportion of all CNBs deemed benign discordant was also similar between institutions. When excluding CNBs from the LAC cohort, this effectively reduced the upgrade rate from 5.5%e2.7% in patients biopsied with VAB. LAC is a public safety-net hospital, with a clinical practice environment in which residents under direct attending supervision undertake much of the radiological evaluation. Norris is a university-based comprehensive cancer center, with attending radiologists conducting all VABs and associated radiologyepathology correlations. We were able to include larger numbers of VAB procedures (n ¼ 63) in our analysis than previous studies, which have ranged from 12e20 patients [11e14]. VAB is more accurate than CNB for initial sampling of lesions suspicious for malignancy, and it is less costly and invasive than EXB for further evaluation of inconclusive or high-risk histology, while largely preserving diagnostic accuracy [6,19e24,29]. In recent years, an increasing number of institutions have recommended VAB for first-line biopsy and repeat VAB as an alternative to EXB for discordance follow-up [19,22,24,30e34]. Only 19 (23.5%) discordant lesions in this study, and none that were ultimately malignant, were evaluated by repeat CNB (Table 1). Of these, only 1 was at Norris and the rest were at LAC. A prior large study of accuracy of CNB demonstrated a significant inverse correlation between rate of sample inadequacy and experience of the operator performing biopsies [35]. We hypothesize that our own findings may be largely due to variable operator experience in the setting of a teaching hospital. The four biopsies in our LAC cohort interpreted as benign but with insufficient tissue may speak to this trend as well. We expect that routine follow-up VAB would have eliminated the need for a portion of the 81 surgeries represented by this cohort. Upgrade rates of overall (6.3%) and LAC-specific (2.7%) benign discordant VABs, compared with a rate of 11.8% for CNBs at LAC, support its superior accuracy in correctly identifying benign lesions. However, these data are

Table 2 e Characteristics of six benign discordant lesions upgraded to malignancy after EXB. Age, y

Clinical presentation

LAC patients 52 Palpable mass 62

Abnormal screening mammogram

51

Suspected Paget disease of the nipple Norris patients 47 Palpable mass 50 48

Abnormal screening mammogram Abnormal screening mammogram

BI-RADS

Core biopsy method

4A

14 G ultrasound-guided CNB 14 G ultrasound-guided CNB

4C

4B

9G MRI-guided VAB

4C

10 G ultrasound-guided VAB 10 G ultrasound-guided VAB 12G ultrasound-guided VAB

4C 5

CNB findings

Final surgical pathology

Fibroadenoma

DCIS

Fibrocystic changes; insufficient glandular tissue for diagnosis Papilloma; pseudoangiomatous stromal hyperplasia

Invasive lobular carcinoma

DCIS

Fibrocystic changes

DCIS

Atypical lobular hyperplasia

DCIS; lobular carcinoma in situ

Pseudoangiomatous stromal hyperplasia

Invasive ductal carcinoma; DCIS

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Table 3 e Final benign histopathologic diagnoses after EXB of discordant lesions. Final diagnosis on surgical pathology

Fibrocystic changes Fibroadenoma Papilloma Sclerosing adenosis Atypical ductal hyperplasia Radial scar/complex sclerosing lesion Other

Frequency, n (%) LAC (n ¼ 52) 15 11 6 3 3 4

(28.8) (21.2) (11.5) (5.8) (5.8) (7.7)

10 (19.2)

Norris (n ¼ 23) 3 5 4 5 3 1

(13.0) (21.7) (17.4) (21.7) (13.0) (4.3)

2 (8.7)

All (n ¼ 75) 18 16 10 8 6 5

(24.0) (21.3) (13.3) (10.7) (8.0) (6.7)

considering repeat VAB as follow-up for discordant biopsies before proceeding to surgery, given the potential for sampling error and delay in diagnosis. Rather than simply broadly supporting or discrediting the routine use of surgery for the management of radiologicepathologic discordant benign breast lesions, we believe that our data may serve to highlight the importance of differences in institutional practice and patient population in evaluating discordance. Given variations in clinical practice and the relative subjectivity of discordance determination, medical centers should examine their practices for performing radiologyepathology correlation when deciding whether to use EXB for discordant lesions.

3 (16.0)

generated from a total of only six instances of malignant upgrade, making it difficult to put forward any specific recommendations for the use of VAB over CNB or EXB. In addition, we must note that using 14-gauge needles with CNB, and larger-bore needles with VAB, likely contributed to the improved accuracy of VAB [12,26,36]. The strong preference for VAB over CNB being performed at Norris prevents a direct comparison of the two methods within our two institutions. The primary strength of our study is that we have assessed the rate of upgrade to malignancy after EXB of the largest cohort of benign discordant VAB needle biopsies to date among studies addressing this question. Our findings indicate that the rate of upgrade to malignancy after VAB in the modern era is 6.3% for a benign discordant lesion, which merits EXB. Our cohort was drawn from a series of 8081 consecutive core-needle breast biopsies performed over a 5.5-y period at two closely affiliated institutionsdone an academic cancer center and the other a public safety-net hospitaldwith a common faculty including dedicated breast imagers. We acknowledge our study’s limitations in that this is a retrospective observational cohort study, with the potential for selection bias. In addition, the low rate of upgrades to malignancy did not allow us to demonstrate any statistically significant associations between clinicopathologic characteristics of discordant breast lesions in our cohort and likelihood of malignant upgrade. In the only other study to include both VAB and CNB, Liberman et al. [12] reported an overall malignancy rate of 24.4%, concluding that discordance is an indication for immediate referral to surgery. As a point of comparison, the clinical management of lobular neoplasia diagnosed on CNB is another debated point in the literature, with the recommendation to perform EXB similarly pivoting on the rate of upgrade to malignancy arrived at by the investigators. This rate has varied from 4.4% to upward of 20%, with the threshold for an author recommending surgical excision appearing to lie somewhere from 5%e10% [37e42]. This contrasts with consistently higher rates of occult malignancy in high-risk lesions such as atypical ductal hyperplasia, leading to their routine removal by EXB [22,43e45]. Our data indicate that the growing utilization of VAB at our institutions has not clearly eliminated the need for EXB, and that EXB remains warranted for radiologicepathologic discordant lesions. At an institution such as LAC reporting a malignancy upgrade rate as low as 5.5%, we suggest

Acknowledgment The authors thank Dr Meade Johnson, Dr Mary Yamashita, and Dr Sandy Lee for their contributions toward accessing and interpreting the data for this study. The project described was supported in part by award number P30CA014089 from the National Cancer Institute. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Cancer Institute or the National Institutes of Health. Author contributions: B.B.P. and L.W. conceived of and designed the study and gathered data. P.S., S.F.S., L.W., and L.L. made vital efforts toward the acquisition of data, with substantial contributions in analysis and interpretation by J.S.W., P.S., S.F.S., L.L., and D.T. B.B.P. drafted the article with significant contributions from J.S.W. and L.W, and all listed authors made meaningful contributions toward critical revision. All authors have approved the article in its current form.

Disclosure The authors report no proprietary or commercial interest in any product mentioned or concept discussed in this article.

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Malignancy rates after surgical excision of discordant breast biopsies.

Vacuum-assisted core-needle biopsy (VAB) is increasingly used to perform breast biopsies instead of automated-gun core-needle biopsy (CNB). The signif...
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