Management of Patients Diagnosed With Lobular Carcinoma in Situ at Needle Core Biopsy at a Community-Based Outpatient Facility

Transcription

1 Women s Imaging Original Research Destounis et al. Management of LCIS Diagnosed at Core Needle Biopsy Women s Imaging Original Research FOCUS ON: Stamatia V. Destounis 1 Philip F. Murphy Posy J. Seifert Patricia A. Somerville Andrea L. Arieno Renee C. Morgan Wende Logan Young Destounis SV, Murphy PF, Seifert PJ, et al. Keywords: breast cancer, breast imaging, lobular carcinoma in situ, needle core biopsy DOI: /AJR Received April 15, 2011; accepted after revision July 21, All authors: Elizabeth Wende Breast Care, LLC, 170 Sawgrass Dr, Rochester, NY Address correspondence to S. V. Destounis (sdestounis@ewbc.com). AJR 2012; 198: X/12/ American Roentgen Ray Society Management of Patients Diagnosed With Lobular Carcinoma in Situ at Needle Core Biopsy at a Community-Based Outpatient Facility OBJECTIVE. The objective of our study was to show the importance of surgical excision after the diagnosis of lobular carcinoma in situ (LCIS) based on needle core biopsy. MATERIALS AND METHODS. Retrospective evaluation of all cases of LCIS diagnosed at needle core biopsy from 2000 to 2011 was performed; 60 patients with 64 diagnoses of LCIS comprise the cohort. Data recorded included patient demographics, patient presentation, breast density, personal and family histories of breast cancer, lesion characteristics, biopsy method, and correlation of core results with surgical pathology or follow-up imaging. The pathology facility was recorded for all biopsies because the specimens from open surgical biopsy were frequently reviewed by a different laboratory. RESULTS. A total of 60 patients with 64 diagnoses of LCIS comprised the study cohort. The patients ranged in age from 36 to 93 years (average, 55 years). The lesions consisted of 39 calcifications, two masses with calcium, 10 masses, two asymmetries, two architectural distortions, two architectural distortions with calcifications, and seven MRI enhancements. Mammography detected lesions in 84% of the cases (n = 54) and 16% (n = 10) were not visualized. Sonography detected lesions in 30% of the cases (n = 19) and 70% (n = 45) were sonographically occult. Needle core biopsy was performed in all cases: 49 stereotactic biopsies (77%), 12 ultrasound-guided biopsies, and three MRI-guided biopsies. All but one case proceeded to surgery. Open surgical biopsy revealed 21 cancers (33%); of the remaining cases, 53% of the cases (n = 33) were atypical or high risk and 14% (n = 9) were benign. CONCLUSION. The diagnosis of LCIS at needle core biopsy, in this small study, revealed that 84% of lesions either were malignant or were atypical or high risk at surgery, of which 33% were found to be carcinoma. Our findings suggest that LCIS should be excised when noted at core biopsy. L obular carcinoma in situ (LCIS) is a noninvasive breast lesion arising from the lobules and the terminal ducts. This type of lesion is characterized by proliferation of generally small and often loosely cohesive cells originating in the terminal duct lobule unit with or without pagetoid involvement of the terminal ducts [1]. Acini are filled with and distended by a solid proliferation of small cells with small, uniform, round-to-oval nuclei with relatively homogeneous chromatin and inconspicuous or absent nucleoli. At least half of the acini in a lobule must be filled with and distended by this cell population to meet the criteria for a diagnosis of LCIS [2]. Proteins that form complexes with E-cadherin at the cell membrane include β-, γ-, α-, and p120-catenins. Reduced expression of E-cadherin has been reported in invasive ductal carcinoma whereas LCIS and invasive lobular carcinoma show complete loss of the protein [3]. LCIS was first described by Foote and Stewart [4] as a cancer lacking clinical signs and was diagnosed once sections of a biopsy specimen were made. LCIS has been thought to be a serendipitous finding, but written reports [5, 6] have shown mammographic findings of calcifications and masses diagnosed as LCIS. With the advances in breast imaging, such as digital mammography and MRI, along with computer-aided detection, the detection of subtle calcifications and masses has become increasingly routine, which has potentially led to the identification of clinical findings diagnosed as LCIS at needle core biopsy. Andersen [7] described in 1977 a 12% increase in breast cancer development once a diagnosis of LCIS was made and recommended careful lifelong follow-up. To this AJR:198, February

2 Destounis et al. day, the management of LCIS remains a topic that continues to be discussed in medical journals, with the treatment of choice ranging from close imaging surveillance, open surgical biopsy, or chemoprophylactic therapy to prophylactic mastectomy [8 10]. This range of treatment strategies has created a controversial scenario for the radiologist: to recommend open surgical biopsy after a core biopsy diagnosis of LCIS or to follow the patient with interval imaging. Because of this controversy, there are no clear guidelines for the management of LCIS diagnosed at needle core biopsy. Needle core biopsy is widely used for the definitive diagnosis of suspicious breast findings and has a reported accuracy rate of 98% [11, 12]. Open surgical biopsy of high-risk lesions, such as atypical ductal hyperplasia, atypical lobular hyperplasia (ALH), radial scar, and LCIS, is often recommended after the initial diagnosis at needle core biopsy. Several studies have shown that the rate of ductal carcinoma in situ (DCIS) or invasive carcinoma had been underestimated at needle core biopsy when subsequent open surgical biopsy was performed of these high-risk lesions [13, 14]. In their early descriptions of LCIS, Foote and Stewart [4] noted that the LCIS process could in some cases be combined with ductal cancers. Because of this possibility, they recommended simple mastectomy. Cohen [15] provided four possible scenarios for the underestimation of these lesions: 1. The target lesion is missed at needle core biopsy and the target represents the malignant lesion that is ultimately diagnosed at open surgical biopsy. 2. An upgrade diagnosis is a reflection of the percentage of malignancies that are not suspected but are diagnosed in addition to the benign lesion that is treated at open surgical biopsy. 3. LCIS is a premalignancy and may evolve into a malignancy. 4. The original diagnosis of lobular neoplasia (i.e., LCIS and ALH) was incorrect and missed DCIS. This review evaluates needle core biopsy diagnosed LCIS cases in depth to seek any radiographic similarities that may help the radiologist with the management of these patients and to determine whether our findings support previous research, which states that when LCIS is diagnosed at needle core biopsy, open surgical biopsy should be recommended [15 20]. In addition, our study proposes to show that, regardless of the biopsy method or needle gauge size, open surgical biopsy is the management of choice to rule out an underlying malignancy. Materials and Methods After receiving institutional review board approval and in compliance with HIPAA, we conducted a retrospective review from the medical records department of all consecutive needle core biopsies performed from February 2000 through January 2011 at an outpatient breast imaging center. From a total of 20,831 needle core biopsies performed during that time period, only patients having a diagnosis of LCIS at needle core biopsy went on for further study analysis. Although LCIS was the primary diagnosis, nine cases were excluded because foci of atypical ductal hyperplasia were found adjacent to the LCIS, resulting in 64 diagnoses of LCIS in 60 patients, a prevalence of 0.3% (n = 64/20,831). Ninety-nine percent (n = 63) of the lesions went on to open surgical biopsy; one patient chose mammographic surveillance due to a previous diagnosis of LCIS. Needle core biopsy was recommended to all patients after a diagnostic workup consisting of mammography, additional mammographic views, ultrasound, and physical examination that resulted in a final assessment of BI-RADS category 4 or 5. The patients were imaged with film-screen mammography (LoRad M4 or LoRad M4 Platinum, Hologic; or Senographe DMR Plus or Senographe 800 T, GE Healthcare) and with full-field digital mammography (LoRad Selenia, Hologic; or Senographe DS, GE Healthcare). An iu22 system (Philips Healthcare), Sonoline Antares system (Siemens Healthcare), or Acuson S2000 system (Siemens Healthcare) was the unit used for the ultrasound evaluations. Needle core biopsies were performed using a dedicated prone stereotactic table (LoRad, Hologic) under ultrasound guidance or with MRI guidance (1.5-T EchoSpeed system, GE Healthcare; or 1.5-T Magnetom Symphony, Siemens Healthcare). For each case, patient demographics including age, menopausal status, hormone status, breast density composition, personal and family histories for breast cancer, and previous breast biopsy history were recorded. Lesion types were categorized and recorded as a mass, calcifications, a mass with calcifications, architectural distortion, architectural distortion and calcifications, a focal asymmetry, and MRI enhancement. The needle core biopsy method for each case was recorded and documented as follows: stereotactic, sonographic, or MRI guidance. Core biopsy needle gauges consisted of 14-gauge automated large-core or 14-, 12-, 11-, or 9-gauge vacuum-assisted devices. All specimens were sent to three local pathology laboratories for review; 60 of 64 went to the same laboratory and four went to other laboratories because of insurance coverage requirements. The experience of the pathologists ranged from 4 to 30 years (average, 17 years); they all used the Page-Rosen-Schnitt criteria for diagnosing LCIS. Histopathology reports of needle core biopsy results were reviewed by the attending radiologist and imaging-pathology correlation was made in all cases. According to our facility protocol when highrisk lesions were diagnosed at needle core biopsy, all cases were referred for open surgical biopsy. The same laboratory was used for needle core biopsy and subsequent open surgical biopsy in 19 cases (30%), and different laboratories were used in 44 cases (70%). The laboratory used for open surgical biopsy was chosen depending on the surgical facility and the surgeons operating privileges. The open surgical biopsy pathology report was also reviewed by the attending radiologist for correlation with needle core biopsy and imaging. Results Study Cohort LCIS was diagnosed in 64 needle core biopsies in 60 patients. The patients ranged in age from 36 to 93 years (average, 55 years) (Table 1). Premenopausal or perimenopausal status was reported by 24 patients and postmenopausal status was reported in 36 patients, seven of whom reported hormone replacement use. A family history of breast cancer was reported by 15 patients (25%) and a previous personal history of breast TABLE 1: Patient Demographics Characteristic No. (%) of Subjects (n = 60) Age (y) (20) (42) (22) (13) > 75 2 (3) Reason for presentation Screening 30 (50) Diagnostic a 31 (52) Breast density Scattered fibroglandular 13 (22) Heterogeneously dense 30 (50) Extremely dense 17 (28) a One patient had a needle core biopsy diagnosis of lobular carcinoma in situ (LCIS) after routine screening; high-risk MRI was recommended at which time a second lesion was identified and diagnosed as LCIS. 282 AJR:198, February 2012

3 Management of LCIS Diagnosed at Core Needle Biopsy cancer was reported by seven patients (12%), all involving the contralateral breast. One patient, in addition to a cancer diagnosis in the contralateral breast, also had a prior diagnosis of LCIS in the ipsilateral breast. TABLE 2: Imaging Findings The recorded breast density was scattered fibroglandular in 13 patients, heterogeneously dense in 30 patients, and dense in 17 patients. A total of 31 screening appointments and 33 diagnostic appointments resulted in the Lesion Type No. (%) of Cases (n = 64) Calcifications 39 (61) Mass with calcium 2 (3) Mass 10 (16) Focal asymmetry 2 (3) Architectural distortion 2 (3) Architectural distortion with calcium 2 (3) MRI enhancement 7 (11) TABLE 3: Core Needle Biopsy Method Variable No. (%) of Cases (n = 64) Image guidance Stereotactic 49 (76.56) Ultrasound 12 (18.75) MRI 3 (4.69) Equipment Directional vacuum-assisted 62 (96.88) 9 16 (25.81) 11 3 (4.84) (64.52) 14 3 (4.84) Automated large-core 2 (3.13) 14 2 (100.0) No. of specimens sampled Mean 7.14 Range specimens 11 (17.19) 6 10 specimens 47 (73.44) 11 specimens 6 (9.38) TABLE 4: Histopathologic Findings From Open Surgical Biopsies Histopathologic Findings Directional Vacuum-Assisted Biopsy No. (%) of Cases (n = 63) Automated Large-Core Biopsy Invasive ductal carcinoma 2 (3.17) 0 Invasive lobular carcinoma 4 (6.35) 0 Ductal carcinoma in situ 14 (22.22) 1 (1.59) Lobular carcinoma in situ 29 (46.03) 1 (1.59) Atypical lobular hyperplasia 3 (4.76) 0 Benign 9 (14.29) 0 finding of 64 LCIS lesions. Four patients had more than one lesion. One patient presented for a diagnostic appointment and bilateral LCIS was found. One patient presented for screening evaluation and two lesions (calcium and an area of architectural distortion not associated with calcium) were identified within the left breast at the 2:00 and 3:00 positions; both were biopsy-proven LCIS. One patient was diagnosed with LCIS at a screening appointment and then on undergoing MRI evaluation had an additional lesion in a different quadrant discovered and diagnosed as LCIS. Last, one patient presented for MRI after a right breast cancer diagnosis and two areas of LCIS were diagnosed in the left breast (10:00 posterior and 8:30 anterior breast). Lesion Detection Of the 31 screening appointments, lesions detected consisted of four masses, 21 calcifications, one mass with calcium, and two architectural distortions, one architectural distortion with calcium, and two asymmetries. In the diagnostic population (33 appointments), lesions consisted of six masses; 18 calcifications; one mass with calcium; one architectural distortion with calcium; and seven MRI enhancements, including six masslike enhancements and one nonmasslike enhancement. Lesion types are reviewed in Table 2. Mammography detected lesions in 84% of cases (n = 54) and 16% (n = 10) were mammographically occult. Of the mammographically occult lesions, seven were detected with ultrasound and three were detected on MRI only. Ultrasound and mammographic correlation was found in 19% of cases (n = 12); 70% (n = 45) were sonographically occult. Ultrasound examinations performed were for diagnostic purposes: because of a finding on mammography, because the patient presented with clinical symptoms, or because of MRI findings. Of the seven MRI enhancements, four were subsequently found at targeted ultrasound and three were visualized only with MRI. The MRI examinations performed were either for high-risk evaluation or for determination of the extent of disease. Needle Core Biopsy Needle core biopsy was performed in all cases (Table 3). As shown by Table 3, 76.56% (n = 49) were biopsied stereotactically; 18.75% (n = 12), with ultrasound guidance; and 4.69% (n = 3), with MRI guidance. Of AJR:198, February

4 Destounis et al. the 62 directional vacuum-assisted biopsies, 40 (65%) were performed with 12-gauge; 16 (26%), with 9-gauge; three (5%), with 11-gauge; and three (5%), with 14-gauge. Automated large-core biopsy was performed in two cases (4%) using a 14-gauge device. The average number of samples for automated large-core biopsies was four and the average number of samples for directional vacuum-assisted biopsies was seven. Open Surgical Biopsy Sixty-three of the 64 lesions (99%) underwent open surgical biopsy and one patient with a prior excision for LCIS chose imaging follow-up rather than further surgery. As shown in Table 4, of the 61 directional vacuum-assisted needle core biopsies that went to surgery, open surgical biopsy pathology revealed that cancer was present in 33% of cases (n = 20): two invasive ductal carcinomas, four invasive lobular carcinomas, and 14 DCIS cases. In 51% of cases (n = 32), there was atypia or high-risk fingings, 29 cases of LCIS and three cases of ALH. In 15% of cases (n = 9), there were benign findings. In the two automated large-core biopsy cases that went to open surgical biopsy, one was DCIS and one had a finding of LCIS. After the initial diagnosis of LCIS at needle core biopsy, open surgical biopsy revealed that 33% of these lesions (n = 21/63) were malignant. Upgrades based on lesion type can be found in Table 5. Although a disproportionate comparison, there was a 50% upgrade rate in lesions sampled with an automated large-core device, with fewer samples taken, versus a 33% upgrade rate in lesions sampled with a directional vacuum-assisted device and more samples taken. Fifteen patients diagnosed with cancer at open surgical biopsy proceeded to lumpectomy and two went on to mastectomy. Of the latter two patients, one underwent bilateral mastectomies because of a core biopsy diagnosis of invasive lobular carcinoma in the right breast and needle core biopsy diagnosis of LCIS in the left breast. This management choice proved beneficial because DCIS previously diagnosed as LCIS at needle core biopsy was found in the left breast at open surgical biopsy. Four patients with needle core biopsy and open surgical biopsy diagnoses of LCIS opted for bilateral prophylactic mastectomies. One patient chose imaging follow-up and did not undergo surgical excision, and to date, there have been no mammographic changes. TABLE 5: Core Needle Biopsy Diagnoses That Were Upgraded Because of Open Surgical Biopsy Findings Lesion Type at Core Needle Biopsy No. (%) of Cases Upgraded Calcifications 14/39 (36) MRI enhancement 2/7 (29) Architectural distortion 1/2 (50) Architectural distortion with calcium 1/2 (50) Mass 2/9 (22) Mass with calcium 1/2 (50) Discussion The Surveillance, Epidemiology, and End Results reported 6974 confirmed cases of LCIS from 2003 through With the diagnosis of LCIS comes an approximate 15% chance of developing an invasive cancer in the breast in which LCIS is found and for developing invasive cancer in the contralateral breast over the subsequent 30 years [6]. Although rare, LCIS has been diagnosed increasingly since the 1980s and currently has an incidence rate of % of core biopsies [21]. With no way of predicting who from this group will have invasive disease, guidelines should be in place when a diagnosis of LCIS is made at needle core biopsy. Georgian-Smith and Lawton [22] conducted a review of the literature and reported a dramatically wide range of malignancy rates: 14%, 16%, 20%, 25%, 37%, and 50%. Hussain and Cunnick [23] reviewed and analyzed pooled data from several studies involving 1229 patients diagnosed with lobular neoplasia on needle core biopsy, of which 263 were LCIS lesions. That review article showed the many various management options that exist when a diagnosis of these lesions is made. The authors concluded that 27% of lobular neoplasia cases were found to contain malignancy on open surgical biopsy and that surgical excision should be considered as the treatment of choice [23]. The radiologist s role when advising patients after a diagnosis of LCIS should be clear, but as these reports show, inconsistency exists, which is why studies to date continue to waver between imaging follow-up and open surgical biopsy. Several published studies support close surveillance over open surgical biopsy [24 27]. Sohn et al. [24] reported that in their study of 50 patients with lobular neoplasia (LCIS or ALH), there were no undiagnosed malignancies in the 21 patients who underwent subsequent surgical excision. Nagi et al. [26] reported that excision is unnecessary if careful radiographic-pathologic correlation is performed and strict histologic criteria are adhered to when making the diagnosis. Maluf and Koerner [28] reported findings that support the opinion that DCIS is the precursor of invasive ductal carcinoma in patients with LCIS: They found that DCIS was frequently seen in specimens containing both LCIS and invasive ductal carcinoma [28]. In our study, six cases were invasive at surgery (two invasive ductal carcinomas and four invasive lobular carcinomas); of these, two were associated with DCIS and four were associated with LCIS. In our small group of invasive cancers diagnosed at open surgical biopsy, we did not find an association with DCIS to be a frequent finding. Studies have shown radiographic evidence that LCIS not only is an incidental finding on biopsy but also is radiographically revealed. A case report presented by Stein et al. [6] shows that LCIS can present clinically and radiologically. In that case, the initial diagnosis was of LCIS, and further analysis of the specimen revealed low-grade DCIS and LCIS. O Driscoll et al. [17] concluded that isolated LCIS on needle core biopsy after mammographic screening is an infrequent finding and may be associated with invasive cancer or DCIS and advise surgical excision of the mammographic abnormality. Our findings are in agreement with those of O Driscoll and colleagues: We also found LCIS to be an infrequent finding given that it accounted for only 0.3% of all of our core biopsy diagnoses during the study period. Like the study by O Driscoll et al., our study found that the rate of cancer diagnosed in these lesions on undergoing open surgical biopsy was substantial, thus supporting our long-standing protocol that all lesions diagnosed as LCIS on needle core biopsy are referred for open surgical biopsy. The results of our small study show that radiographic findings were present in a majority 284 AJR:198, February 2012

5 Management of LCIS Diagnosed at Core Needle Biopsy A of histopathologically confirmed cases of LCIS at needle core biopsy, given that 54 of the 64 lesions were visualized mammographically (Figs. 1 and 2). Ten lesions were not radiographically visualized: Seven MRI enhancements and three masses were seen only with ultrasound. Of these 54 lesions, 43 presented as calcifications alone or were associated with calcifications. The pathologist identified calcium with LCIS in 35 of the 43 specimens, thus supporting studies that calcifications can be associated with LCIS [5, 29]. At open surgical biopsy, 12 of the 35 cases of calcifications or lesions associated with calcifications were malignant. In the screening environment, all of the lesions except one were seen on mammograms. In the diagnostic setting, 16 of the cases with radiographic findings in this study cohort presented as second opinions from outside facilities; from reviewing records, we deduced that at least two referring physicians were worried about the mammographic findings. Of these 16 cases, two ill-defined masses, 12 new calcifications, and one architectural distortion with calcium were given BI-RADS category 4 assessments. One patient had cysts associated with calcium diagnosed as BI-RADS category 3. This patient opted for a second opinion rather than shortterm follow-up. Two of these second-opinion cases (13%) were upgraded to carcinoma (both DCIS) at surgery. Of the remaining B 17, mammography detected calcifications in five cases and a mass in one case. Three masses were visualized with ultrasound only and seven MRI enhancements were identified (one patient with two lesions). These findings contradict the belief that LCIS is a chance finding during biopsy. Brem et al. [14] found that the diagnosis of lobular neoplasia was an underestimation of cancer in 23% of cases specifically, a 25% rate for LCIS. Our findings are in line with their results because cancer was diagnosed in our study in 33% of the cases at open surgical biopsy, therefore showing that open surgical biopsy should be recommended after a core diagnosis of LCIS. With the needle core Fig year-old woman who presented for routine screening mammography. A and B, Mammographic craniocaudal (A) and mediolateral oblique (B) views show irregular mass (arrow) with pleomorphic calcifications in left 1:30 area. C, Magnification view shows mass (arrow) with irregular microcalcifications. D, Ultrasound image reveals subtle, hypoechoic, ovoid-shaped, 2-cm mass (arrow) containing numerous echogenic foci. E, Ultrasound-guided needle core biopsy image reveals lobular carcinoma in situ. At open surgical biopsy, diagnosis of infiltrating lobular carcinoma was made. C D E AJR:198, February

6 Destounis et al. biopsy diagnosis of LCIS, the open surgical recommendation was strongly followed; in this study, only one patient chose imaging follow-up because of a previous diagnosis of LCIS at open surgical biopsy. There were limitations with this study. A variety of needle gauges were used for the A C E needle core biopsies. The use of one needle gauge would have limited this variable. Also, different pathology laboratories were used for the needle core biopsy diagnosis and open surgical biopsy diagnosis. The use of one laboratory and one pathologist would have been ideal for continuity. For the calcium cases, B D Fig year-old woman who presented for routine screening mammography. A D, Mammographic views (A and B) and magnified views (C and D) show area of diffuse amorphous and pleomorphic calcifications (arrows, D). Needle core biopsy revealed lobular carcinoma in situ. E and F, Breast MRI was performed to determine extent of disease. Sagittal T1 fat-saturated gadolinium-enhanced image (E) and maximumintensity-projection image (F) reveal diffuse enhancement throughout left breast, measuring 6 cm in greatest dimension. On surgical excision, diagnosis of infiltrating ductal carcinoma was made. F the pathology review did not always specify if calcifications were in the midst of the LCIS. It would have been ideal for this review if that information had been specified for each case. Because this review was conducted at an outpatient breast imaging center, the radiologists did not have pathology 286 AJR:198, February 2012

7 Management of LCIS Diagnosed at Core Needle Biopsy slides readily available for review after open surgical biopsy, which limited the ability to determine the relationship of the cancer to the needle core biopsy diagnosis of LCIS. In addition, this review consisted of a small subset of patients, which hinders the ability to prove statistical significance. Even with the small numbers retrospectively reviewed in this study, open surgical biopsy proved beneficial, revealing a diagnosis of cancer in 21 patients. A larger study with all radiographically shown lesions diagnosed at needle core biopsy as LCIS would be beneficial because it could identify trends of radiographic indicators to help the radiologist recommend surgery or imaging surveillance in the management of this high-risk marker. References 1. Mulheron B, Gray R, Packaj B, et al. Is excisional biopsy indicated for patients with lobular neoplasia diagnosed on percutaneous core needle biopsy of the breast? Am J Surg 2009; 198: Brogi E, Murray MP, Corben AD. Lobular carcinoma, not only a classic. Breast J 2010; 16(suppl 1):S10 S14 3. Mastracci T, Tjan S, Bane A, et al. E-cadherin alterations in atypical lobular hyperplasia and lobular carcinoma in situ of the breast. Mod Pathol 2005; 18: Foote FW, Stewart FW. Lobular carcinoma in situ: a rare form of mammary cancer. Am J Pathol 1941; 73: Georgian-Smith D, Lawton TJ. Calcifications of lobular carcinoma in situ of the breast: radiologicpathologic correlation. AJR 2001; 176: Stein LF, Gilat Z, Rapelyea JA, Schwartz AM, Abell B, Brem RF. Lobular carcinoma in situ of the breast presenting as a mass. AJR 2005; 184: Andersen JA. Lobular carcinoma in situ of the breast: an approach to rational treatment. Cancer 1977; 39: Osborne MP, Hoda SA. Current management of lobular carcinoma in situ of the breast. Oncology 1994; 8: Carson W, Sanchez-Forgach E, Stomper P, Penetrante R, Tsangaris TN, Edge SB. Lobular carcinoma in situ: observation without surgery as an appropriate therapy. Ann Surg Oncol 1994; 1: Gump FE, Kinne D, Schwartz GF. Current treatment for lobular carcinoma in situ. Ann Surg Oncol 1998; 5: Jackman RJ, Nowels K, Rodriguez-Soto J, et al. Stereotactic, automated, large-core needle biopsy of nonpalpable breast lesions: false-negative and histologic underestimation rates after long-term follow-up. Radiology 1999; 210: Liberman L. Percutaneous image-guided core biopsy. Radiol Clin North Am 2002; 40: Berg WA. Image-guided breast biopsy and management of high-risk lesions. Radiol Clin North Am 2004; 42: , vii 14. Brem RF, Lechner MC, Jackman RJ, et al. Lobular neoplasia at percutaneous breast biopsy: variables associated with carcinoma at surgical excision. AJR 2008; 190: Cohen MA. Cancer upgrades at excisional biopsy after diagnosis of atypical lobular hyperplasia or lobular carcinoma in situ at core-needle biopsy: some reasons why. Radiology 2004; 231: Liberman L, Sama M, Susnik B, et al. Lobular carcinoma in situ at percutaneous breast biopsy: surgical biopsy findings. AJR 1999; 173: O Driscoll D, Britton P, Borrow L, et al. Lobular carcinoma in situ on core biopsy: what is the clinical significance? Clin Radiol 2001; 56: Shin SJ, Rose PP. Excisional biopsy should be performed if lobular carcinoma in situ is seen on needle core biopsy. Arch Pathol Lab Med 2002; 126: Foster MC, Helvie MA, Gregory NE, Rebner M, Nees AV, Paramagul C. Lobular carcinoma in situ or atypical lobular hyperplasia at core-needle biopsy: is excisional biopsy necessary? Radiology 2004; 231: Middleton L, Grant S, Stephens T, et al. Lobular carcinoma in situ diagnosed by core needle biopsy: when should it be excised? Mod Pathol 2003; 16: Esserman L, Lamea L, Tanev S, et al. Should the extent of lobular neoplasia on core biopsy influence the decision for excision? Breast J 2007; 13: Georgian-Smith D, Lawton TJ. Controversies on the management of high-risk lesions at core biopsy from a radiology/pathology perspective. Radiol Clin North Am 2010; 48: Hussain M, Cunnick GH. Management of lobular carcinoma in situ and atypical lobular hyperplasia of the breast: a review. Eur J Surg Oncol 2011; 37: Sohn V, Arthurs Z, Kim F, et al. Lobular neoplasia: is surgical excision warranted? Am Surg 2008; 74: Renshaw A, Cartagena N, Derhagopian R, Gould EW. Lobular neoplasia in breast core needle biopsy specimens is not associated with an increased risk of ductal carcinoma in situ or invasive carcinoma. Am J Clin Pathol 2002; 117: Nagi C, O Donnell J, Tismenetsky M, et al. Lobular neoplasia on core needle biopsy does not require excision. Cancer 2008; 112: Hwang H, Barke L, Mendelson E, et al. Atypical lobular hyperplasia and classic lobular carcinoma in situ in core biopsy specimens: routine excision is not necessary. Mod Pathol 2008; 21: Maluf H, Koerner F. Lobular carcinoma in situ and infiltrating ductal carcinoma: frequent presence of DCIS as a precursor lesion. Int J Surg Pathol 2001; 9: Purdie C, McLean D, Stormonth E, et al. Management of in situ lobular neoplasia detected on needle core biopsy of breast. J Clin Pathol 2010; 63: AJR:198, February