High-risk lesions of the breast: concurrent diagnostic tools and management recommendations

Francesca Catanzariti1, Daly Avendaño2, Giuseppe Cicero1, Margarita Garza-Montemayor2, Sofia Chrisafi1, Emmanuele Venanzi Rullo3, Giorgio Ascenti1, Katja Pinker-Domenig4, Maria Adele Marino1
1Department of Biomedical Sciences and Morphologic and Functional Imaging, University of Messina, Messina, Italy
2Department of Breast Imaging, Breast Cancer Center TecSalud, ITESM Monterrey, Nuevo Leon, Mexico
3Unit of Infectious Diseases, Department of Clinical and Experimental Medicine, University of Messina, 98124, Messina, Italy
4Department of Radiology, Breast Imaging Service, Memorial Sloan Kettering Cancer Center, Suite 705, 300 E 66th Street, New York, NY, 10065, USA

Tóm tắt

AbstractBreast lesions with uncertain malignant behavior, also known as high-risk or B3 lesions, are composed of a variety of pathologies with differing risks of associated malignancy. While open excision was previously preferred to manage all high-risk lesions, tailored management has been increasingly favored to reduce overtreatment and spare patients from unnecessary anxiety or high healthcare costs associated with surgical excision. The purpose of this work is to provide the reader with an accurate overview focused on the main high-risk lesions of the breast: atypical intraductal epithelial proliferation (atypical ductal hyperplasia), lobular neoplasia (including the subcategories lobular carcinoma in situ and atypical lobular hyperplasia), flat epithelial atypia, radial scar and papillary lesions, and phyllodes tumor. Beyond merely presenting the radiological aspects of these lesions and the recent literature, information about their potential upgrade rates is discussed in order to provide a useful guide for appropriate clinical management while avoiding the risks of unnecessary surgical intervention (overtreatment).

Từ khóa


Tài liệu tham khảo

Clauser P, Kapetas P, Stöttinger A et al (2020) A risk stratification algorithm for lesions of uncertain malignant potential diagnosed by vacuum-assisted breast biopsy (VABB) of mammographic microcalcifications. Eur J Radiol 135:109479. https://doi.org/10.1016/j.ejrad.2020.109479

Vizcaíno I, Gadea L, Andreo L et al (2001) Short-term follow-up results in 795 nonpalpable probably benign lesions detected at screening mammography. Radiology 219:475–483. https://doi.org/10.1148/radiology.219.2.r01ma11475

D’Orsi CJ, Sickles EA, Mendelson EB et al (2013) ACR BI-RADS® Atlas, breast imaging reporting and data system. American College of Radiology, Reston

Bianchi S, Caini S, Renne G et al (2011) Positive predictive value for malignancy on surgical excision of breast lesions of uncertain malignant potential (B3) diagnosed by stereotactic vacuum-assisted needle core biopsy (VANCB): a large multi-institutional study in Italy. Breast 20:264–270. https://doi.org/10.1016/j.breast.2010.12.003

Rageth CJ, O’Flynn EAM, Pinker K et al (2019) Second international conference on lesions of uncertain malignant potential in the breast (B3 lesions). Breast Cancer Res Treat 174:279–296. https://doi.org/10.1007/s10549-018-05071-1

Shaaban AM, Sharma N (2019) Management of B3 lesions—practical issues. Curr Breast Cancer Rep 11:83–88. https://doi.org/10.1007/s12609-019-0310-6

Thomas PS (2018) Diagnosis and management of high-risk breast lesions. J Natl Compr Cancer Netw 16:1391–1396. https://doi.org/10.6004/jnccn.2018.7099

Coopey SB, Mazzola E, Buckley JM et al (2012) The role of chemoprevention in modifying the risk of breast cancer in women with atypical breast lesions. Breast Cancer Res Treat 136:627–633. https://doi.org/10.1007/s10549-012-2318-8

Heywang-Köbrunner SH, Nährig J, Hacker A, Sedlacek S, Höfler H (2010) B3 lesions: radiological assessment and multi-disciplinary aspects. Breast Care (Basel) 5:209–217. https://doi.org/10.1159/000319326

El‐Sayed ME, Rakha EA, Reed J, Lee AHS, Evans AJ, Ellis IO (2008) Predictive value of needle core biopsy diagnoses of lesions of uncertain malignant potential (B3) in abnormalities detected by mammographic screening. Histopathology 53:650–657. https://doi.org/10.1111/j.1365-2559.2008.03158.x

Pinder SE, Shaaban A, Deb R et al (2018) NHS breast screening multidisciplinary working group guidelines for the diagnosis and management of breast lesions of uncertain malignant potential on core biopsy (B3 lesions). Clin Radiol 73:682–692. https://doi.org/10.1016/j.crad.2018.04.004

Alonso-Bartolomé P, Vega-Bolívar A, Torres-Tabanera M et al (2004) Sonographically guided 11-G directional vacuum-assisted breast biopsy as an alternative to surgical excision: utility and cost study in probably benign lesions. Acta Radiol 45:390–396

Saladin C, Haueisen H, Kampmann G et al (2016) Lesions with unclear malignant potential (B3) after minimally invasive breast biopsy: evaluation of vacuum biopsies performed in Switzerland and recommended further management. Acta Radiol 57:815–821. https://doi.org/10.1177/0284185115610931

Rageth CJ, Flynn EA, Comstock C et al (2016) First international consensus conference on lesions of uncertain malignant potential in the breast (B3 lesions). Breast Cancer Res Treat 159:203–213. https://doi.org/10.1007/s10549-016-3935-4

Forester ND, Lowes S, Mitchell E, Twiddy M (2019) High risk (B3) breast lesions: what is the incidence of malignancy for individual lesion subtypes? A systematic review and meta-analysis. Eur J Surg Oncol 45:519–527. https://doi.org/10.1016/j.ejso.2018.12.008

Brem RF (2020) Management of breast atypical ductal hyperplasia: now and the future. Radiology 294:87–88. https://doi.org/10.1148/radiol.2019192192

Lewin AA, Mercado CL (2020) Atypical ductal hyperplasia and lobular neoplasia: update and easing of guidelines. AJR Am J Roentgenol 214:265–275. https://doi.org/10.2214/AJR.19.21991

Lakhani SREI, Schnitt SJ, Tan PH, van de Vijver MJ (2012) WHO classification of tumours of the breast, fourth edition 2012. International Agency for Research on Cancer, Lyon

Grippo C, Jagmohan P, Clauser P et al (2020) External validation of a risk stratification score for B3 breast lesions detected at ultrasound core needle biopsy. Diagnostics. https://doi.org/10.3390/diagnostics10040181

Mooney KL, Bassett LW, Apple SK (2016) Upgrade rates of high-risk breast lesions diagnosed on core needle biopsy: a single-institution experience and literature review. Mod Pathol 29:1471–1484. https://doi.org/10.1038/modpathol.2016.127

Eby PR, Ochsner JE, DeMartini WB, Allison KH, Peacock S, Lehman CD (2009) Frequency and upgrade rates of atypical ductal hyperplasia diagnosed at stereotactic vacuum-assisted breast biopsy: 9-versus 11-gauge. AJR Am J Roentgenol 192:229–234. https://doi.org/10.2214/AJR.08.1342

Choi J, Koo JS (2012) Comparative study of histological features between core needle biopsy and surgical excision in phyllodes tumor. Pathol Int 62:120–126. https://doi.org/10.1111/j.1440-1827.2011.02761.x

Margenthaler JA, Duke D, Monsees BS, Barton PT, Clark C, Dietz JR (2006) Correlation between core biopsy and excisional biopsy in breast high-risk lesions. Am J Surg 192:534–537. https://doi.org/10.1016/j.amjsurg.2006.06.003

Lamb LR, Bahl M, Hughes KS, Lehman CD (2018) Pathologic upgrade rates of high-risk breast lesions on digital two-dimensional vs tomosynthesis mammography. J Am Coll Surg 226:858–867. https://doi.org/10.1016/j.jamcollsurg.2017.12.049

Quinn EM, Dunne E, Flanagan F et al (2020) Radial scars and complex sclerosing lesions on core needle biopsy of the breast: upgrade rates and long-term outcomes. Breast Cancer Res Treat 183:677–682. https://doi.org/10.1007/s10549-020-05806-z

Speer ME, Huang ML, Dogan BE et al (2018) High risk breast lesions identified on MRI-guided vacuum-assisted needle biopsy: outcome of surgical excision and imaging follow-up. Br J Radiol 91:20180300. https://doi.org/10.1259/bjr.20180300

Otterbach F, Bankfalvi A, Bergner S, Decker T, Krech R, Boecker W (2000) Cytokeratin 5/6 immunohistochemistry assists the differential diagnosis of atypical proliferations of the breast. Histopathology 37:232–240. https://doi.org/10.1046/j.1365-2559.2000.00882.x

Boecker W, van Horn L, Stenman G et al (2018) Spatially correlated phenotyping reveals K5-positive luminal progenitor cells and p63–K5/14-positive stem cell-like cells in human breast epithelium. Lab Invest 98:1065–1075. https://doi.org/10.1038/s41374-018-0054-3

Lopez‐Garcia MA, Geyer FC, Lacroix‐Triki M, Marchió C, Reis‐Filho JS (2010) Breast cancer precursors revisited: molecular features and progression pathways. Histopathology 57:171–192. https://doi.org/10.1111/j.1365-2559.2010.03568.x

Clauser P, Marino MA, Baltzer PAT, Bazzocchi M, Zuiani C (2016) Management of atypical lobular hyperplasia, atypical ductal hyperplasia, and lobular carcinoma in situ. Expert Rev Anticancer Ther 16:335–346. https://doi.org/10.1586/14737140.2016.1143362

Hartmann LC, Radisky DC, Frost MH et al (2014) Understanding the premalignant potential of atypical hyperplasia through its natural history: a longitudinal cohort study. Cancer Prev Res (Phila) 7:211–217. https://doi.org/10.1158/1940-6207.CAPR-13-0222

Mesurolle B, Perez JCH, Azzumea F et al (2014) Atypical ductal hyperplasia diagnosed at sonographically guided core needle biopsy: frequency, final surgical outcome, and factors associated with underestimation. AJR Am J Roentgenol 202:1389–1394. https://doi.org/10.2214/AJR.13.10864

Heller SL, Elias K, Gupta A, Greenwood HI, Mercado CL, Moy L (2014) Outcome of high-risk lesions at MRI-guided 9-gauge vacuum-assisted breast biopsy. AJR Am J Roentgenol 202:237–245. https://doi.org/10.2214/AJR.13.10600

Kohr JR, Eby PR, Allison KH et al (2010) Risk of upgrade of atypical ductal hyperplasia after stereotactic breast biopsy: effects of number of foci and complete removal of calcifications. Radiology 255:723–730. https://doi.org/10.1148/radiol.09091406

Upgrade rate of percutaneously diagnosed pure atypical ductal hyperplasia: systematic review and meta-analysis of 6458 Lesions|Radiology. https://doi.org/10.1148/radiol.2019190748. Accessed 23 Sep 2020

Ko E, Han W, Lee JW et al (2008) Scoring system for predicting malignancy in patients diagnosed with atypical ductal hyperplasia at ultrasound-guided core needle biopsy. Breast Cancer Res Treat 112:189–195. https://doi.org/10.1007/s10549-007-9824-0

Monticciolo DL, Newell MS, Moy L, Niell B, Monsees B, Sickles EA (2018) Breast cancer screening in women at higher-than-average risk: recommendations from the ACR. J Am Coll Radiol 15:408–414. https://doi.org/10.1016/j.jacr.2017.11.034

Choi BB, Kim SH, Shu KS (2012) Lobular lesions of the breast: imaging findings of lobular neoplasia and invasive lobular carcinoma. J Reprod Med 57:26–34

Liberman L, Sama M, Susnik B et al (1999) Lobular carcinoma in situ at percutaneous breast biopsy: surgical biopsy findings. AJR Am J Roentgenol 173:291–299. https://doi.org/10.2214/ajr.173.2.10430122

Ginter PS, D’Alfonso TM (2017) Current concepts in diagnosis, molecular features, and management of lobular carcinoma in situ of the breast with a discussion of morphologic variants. Arch Pathol Lab Med 141:1668–1678. https://doi.org/10.5858/arpa.2016-0421-RA

Ditsch N, Untch M, Thill M et al (2019) AGO recommendations for the diagnosis and treatment of patients with early breast cancer: update 2019. Breast Care (Basel) 14:224–245. https://doi.org/10.1159/000501000

Malhaire C, El Khoury C, Thibault F et al (2010) Vacuum-assisted biopsies under MR guidance: results of 72 procedures. Eur Radiol 20:1554–1562. https://doi.org/10.1007/s00330-009-1707-9

Chuba PJ, Hamre MR, Yap J et al (2005) Bilateral risk for subsequent breast cancer after lobular carcinoma-in-situ: analysis of surveillance, epidemiology, and end results data. J Clin Oncol 23:5534–5541. https://doi.org/10.1200/JCO.2005.04.038

Fisher ER, Land SR, Fisher B, Mamounas E, Gilarski L, Wolmark N (2004) Pathologic findings from the National Surgical Adjuvant Breast and Bowel Project: twelve-year observations concerning lobular carcinoma in situ. Cancer 100:238–244. https://doi.org/10.1002/cncr.11883

IA Cancer for R on Organization WH (2003) Pathology and genetics of tumours of the breast and female genital organs. IARC, Lyon

Fasola CE, Chen JJ, Jensen KC, Allison KH, Horst KC (2018) Characteristics and clinical outcomes of pleomorphic lobular carcinoma in situ of the breast. Breast J 24:66–69. https://doi.org/10.1111/tbj.12843

Dabbs DJ, Schnitt SJ, Geyer FC et al (2013) Lobular neoplasia of the breast revisited with emphasis on the role of E-cadherin immunohistochemistry. Am J Surg Pathol 37:e1-11. https://doi.org/10.1097/PAS.0b013e3182918a2b

Murray MP, Luedtke C, Liberman L, Nehhozina T, Akram M, Brogi E (2013) Classic lobular carcinoma in situ and atypical lobular hyperplasia at percutaneous breast core biopsy: outcomes of prospective excision. Cancer 119:1073–1079. https://doi.org/10.1002/cncr.27841

Atkins KA, Cohen MA, Nicholson B, Rao S (2013) Atypical lobular hyperplasia and lobular carcinoma in situ at core breast biopsy: use of careful radiologic-pathologic correlation to recommend excision or observation. Radiology 269:340–347. https://doi.org/10.1148/radiol.13121730

Genco IS, Tugertimur B, Chang Q, Cassell L, Hajiyeva S (2020) Outcomes of classic lobular neoplasia diagnosed on breast core needle biopsy: a retrospective multi-center study. Virchows Arch 476:209–217. https://doi.org/10.1007/s00428-019-02685-8

Page DL, Dupont WD, Rogers LW, Rados MS (1985) Atypical hyperplastic lesions of the female breast. A long-term follow-up study. Cancer 55:2698–2708. https://doi.org/10.1002/1097-0142(19850601)55:11%3c2698::aid-cncr2820551127%3e3.0.co;2-a

Beute BJ, Kalisher L, Hutter RV (1991) Lobular carcinoma in situ of the breast: clinical, pathologic, and mammographic features. AJR Am J Roentgenol 157:257–265. https://doi.org/10.2214/ajr.157.2.1853802

Georgian-Smith D, Lawton TJ (2001) Calcifications of lobular carcinoma in situ of the breast: radiologic-pathologic correlation. AJR Am J Roentgenol 176:1255–1259. https://doi.org/10.2214/ajr.176.5.1761255

Ferré R, Omeroglu A, Mesurolle B (2017) Sonographic appearance of lesions diagnosed as lobular neoplasia at sonographically guided biopsies. AJR Am J Roentgenol 208:669–675. https://doi.org/10.2214/AJR.15.15056

Rendi MH, Dintzis SM, Lehman CD, Calhoun KE, Allison KH (2012) Lobular in-situ neoplasia on breast core needle biopsy: imaging indication and pathologic extent can identify which patients require excisional biopsy. Ann Surg Oncol 19:914–921. https://doi.org/10.1245/s10434-011-2034-3

Liberman L, Drotman M, Morris EA et al (2000) Imaging-histologic discordance at percutaneous breast biopsy. Cancer 89:2538–2546. https://doi.org/10.1002/1097-0142(20001215)89:12%3c2538::aid-cncr4%3e3.0.co;2-#

Liberman L, Holland AE, Marjan D et al (2007) Underestimation of atypical ductal hyperplasia at MRI-guided 9-gauge vacuum-assisted breast biopsy. Am J Roentgenol 188:684–690. https://doi.org/10.2214/AJR.06.0809

Schmidt H, Arditi B, Wooster M et al (2018) Observation versus excision of lobular neoplasia on core needle biopsy of the breast. Breast Cancer Res Treat 168:649–654. https://doi.org/10.1007/s10549-017-4629-2

Shah-Khan MG, Geiger XJ, Reynolds C, Jakub JW, DePeri ER, Glazebrook KN (2012) Long-term follow-up of lobular neoplasia (atypical lobular hyperplasia/lobular carcinoma in situ) diagnosed on core needle biopsy. Ann Surg Oncol 19:3131–3138. https://doi.org/10.1245/s10434-012-2534-9

Schiaffino S, Gristina L, Villa A et al (2018) Flat epithelial atypia: conservative management of patients without residual microcalcifications post-vacuum-assisted breast biopsy. Br J Radiol. https://doi.org/10.1259/bjr.20170484

Lerwill MF (2008) Flat epithelial atypia of the breast. Arch Pathol Lab Med 132:615–621. https://doi.org/10.1043/1543-2165(2008)132[615:FEAOTB]2.0.CO;2

Sotiriou C, Neo S-Y, McShane LM et al (2003) Breast cancer classification and prognosis based on gene expression profiles from a population-based study. Proc Natl Acad Sci U S A 100:10393–10398. https://doi.org/10.1073/pnas.1732912100

Bombonati A, Sgroi DC (2011) The molecular pathology of breast cancer progression. J Pathol 223:307–317. https://doi.org/10.1002/path.2808

Rudin AV, Hoskin TL, Fahy A et al (2017) Flat epithelial atypia on core biopsy and upgrade to cancer: a systematic review and meta-analysis. Ann Surg Oncol 24:3549–3558. https://doi.org/10.1245/s10434-017-6059-0

Schnitt SJ (2003) The diagnosis and management of pre-invasive breast disease: flat epithelial atypia–classification, pathologic features and clinical significance. Breast Cancer Res 5:263–268. https://doi.org/10.1186/bcr625

Schnitt SJ, Vincent-Salomon A (2003) Columnar cell lesions of the breast. Adv Anat Pathol 10:113–124. https://doi.org/10.1097/00125480-200305000-00001

Elston CW, Sloane JP, Amendoeira I et al (2000) Causes of inconsistency in diagnosing and classifying intraductal proliferations of the breast. European Commission Working Group on breast screening pathology. Eur J Cancer 36:1769–1772. https://doi.org/10.1016/s0959-8049(00)00181-7

Said SM, Visscher DW, Nassar A et al (2015) Flat epithelial atypia and risk of breast cancer: a Mayo cohort study. Cancer 121:1548–1555. https://doi.org/10.1002/cncr.29243

Kunju LP, Kleer CG (2007) Significance of flat epithelial atypia on mammotome core needle biopsy: should it be excised? Hum Pathol 38:35–41. https://doi.org/10.1016/j.humpath.2006.08.008

Khoumais NA, Scaranelo AM, Moshonov H et al (2013) Incidence of breast cancer in patients with pure flat epithelial atypia diagnosed at core-needle biopsy of the breast. Ann Surg Oncol 20:133–138. https://doi.org/10.1245/s10434-012-2591-0

Solorzano S, Mesurolle B, Omeroglu A et al (2011) Flat epithelial atypia of the breast: pathological-radiological correlation. AJR Am J Roentgenol 197:740–746. https://doi.org/10.2214/AJR.10.5265

Ceugnart L, Doualliez V, Chauvet M-P et al (2013) Pure flat epithelial atypia: is there a place for routine surgery? Diagn Interv Imaging 94:861–869. https://doi.org/10.1016/j.diii.2013.01.011

Villa A, Chiesa F, Massa T et al (2013) Flat epithelial atypia: comparison between 9-gauge and 11-gauge devices. Clin Breast Cancer 13:450–454. https://doi.org/10.1016/j.clbc.2013.08.008

Crystal P, Sadaf A, Bukhanov K, McCready D, O’Malley F, Helbich TH (2011) High-risk lesions diagnosed at MRI-guided vacuum-assisted breast biopsy: can underestimation be predicted? Eur Radiol 21:582–589. https://doi.org/10.1007/s00330-010-1949-6

Heller SL, Moy L (2012) Imaging features and management of high-risk lesions on contrast-enhanced dynamic breast MRI. Am J Roentgenol 198:249–255. https://doi.org/10.2214/AJR.11.7610

Lucioni M, Rossi C, Lomoro P et al (2020) Positive predictive value for malignancy of uncertain malignant potential (B3) breast lesions diagnosed on vacuum-assisted biopsy (VAB): is surgical excision still recommended? Eur Radiol. https://doi.org/10.1007/s00330-020-07161-5

DiPasquale A, Silverman S, Farag E, Peiris L (2020) Flat epithelial atypia: are we being too aggressive? Breast Cancer Res Treat 179:511–517. https://doi.org/10.1007/s10549-019-05481-9

Chou WYY, Veis DJ, Aft R (2018) Radial scar on image-guided breast biopsy: is surgical excision necessary? Breast Cancer Res Treat 170:313–320. https://doi.org/10.1007/s10549-018-4741-y

Wellings SR, Alpers CE (1984) Subgross pathologic features and incidence of radial scars in the breast. Hum Pathol 15:475–479. https://doi.org/10.1016/s0046-8177(84)80083-0

Alleva DQ, Smetherman DH, Farr GH, Cederbom GJ (1999) Radial scar of the breast: radiologic-pathologic correlation in 22 cases. Radiographics 19:S27–S35. https://doi.org/10.1148/radiographics.19.suppl_1.g99oc05s27

Cohen MA, Newell MS (2017) Radial scars of the breast encountered at core biopsy: review of histologic, imaging, and management considerations. Am J Roentgenol 209:1168–1177. https://doi.org/10.2214/AJR.17.18156

Alvarado-Cabrero I, Tavassoli FA (2000) Neoplastic and malignant lesions involving or arising in a radial scar: a clinicopathologic analysis of 17 cases. Breast J 6:96–102

López-Medina A, Cintora E, Múgica B, Operé E, Vela AC, Ibañez T (2006) Radial scars diagnosed at stereotactic core-needle biopsy: surgical biopsy findings. Eur Radiol 16:1803–1810. https://doi.org/10.1007/s00330-006-0196-3

Tran H-T, Mursleen A, Mirpour S, Ghanem O, Farha MJ (2017) Papillary breast lesions: association with malignancy and upgrade rates on surgical excision. Am Surg 83:1294–1297

Wyss P, Varga Z, Rössle M, Rageth CJ (2014) Papillary lesions of the breast: outcomes of 156 patients managed without excisional biopsy. Breast J 20:394–401. https://doi.org/10.1111/tbj.12283

Yamaguchi R, Tanaka M, Tse GM et al (2015) Management of breast papillary lesions diagnosed in ultrasound-guided vacuum-assisted and core needle biopsies. Histopathology 66:565–576. https://doi.org/10.1111/his.12477

Teaching Atlas of Mammography. https://www.thieme.com/books-main/radiology/product/80-teaching-atlas-of-mammography. Accessed 17 Jul 2020

Orel SG, Evers K, Yeh IT, Troupin RH (1992) Radial scar with microcalcifications: radiologic-pathologic correlation. Radiology 183:479–482. https://doi.org/10.1148/radiology.183.2.1561353

Skaane P (2017) Breast cancer screening with digital breast tomosynthesis. Breast Cancer 24:32–41. https://doi.org/10.1007/s12282-016-0699-y

Houssami N, Skaane P (2013) Overview of the evidence on digital breast tomosynthesis in breast cancer detection. Breast 22:101–108. https://doi.org/10.1016/j.breast.2013.01.017

Partyka L, Lourenco AP, Mainiero MB (2014) Detection of mammographically occult architectural distortion on digital breast tomosynthesis screening: initial clinical experience. Am J Roentgenol 203:216–222. https://doi.org/10.2214/AJR.13.11047

Pujara AC, Hui J, Wang LC (2019) Architectural distortion in the era of digital breast tomosynthesis: outcomes and implications for management. Clin Imaging 54:133–137. https://doi.org/10.1016/j.clinimag.2019.01.004

Andacoglu O, Kanbour-Shakir A, Teh Y-C et al (2013) Rationale of excisional biopsy after the diagnosis of benign radial scar on core biopsy: a single institutional outcome analysis. Am J Clin Oncol 36:7–11. https://doi.org/10.1097/COC.0b013e3182354a3f

Shetty MK (2002) Radial scars of the breast: sonographic findings. Ultrasound Q 18:203–207. https://doi.org/10.1097/00013644-200209000-00005

Park VY, Kim E-K, Kim MJ, Yoon JH, Moon HJ (2016) Mammographically occult asymptomatic radial scars/complex sclerosing lesions at ultrasonography-guided core needle biopsy: follow-up can be recommended. Ultrasound Med Biol 42:2367–2371. https://doi.org/10.1016/j.ultrasmedbio.2016.06.004

Ha SM, Cha JH, Shin HJ et al (2018) Radial scars/complex sclerosing lesions of the breast: radiologic and clinicopathologic correlation. BMC Med Imaging 18:39. https://doi.org/10.1186/s12880-018-0279-z

Eiada R, Chong J, Kulkarni S, Goldberg F, Muradali D (2012) Papillary lesions of the breast: MRI, ultrasound, and mammographic appearances. Am J Roentgenol 198:264–271. https://doi.org/10.2214/AJR.11.7922

Collins LC, Schnitt SJ (2008) Papillary lesions of the breast: selected diagnostic and management issues. Histopathology 52:20–29. https://doi.org/10.1111/j.1365-2559.2007.02898.x

Nakhlis F (2018) How do we approach benign proliferative lesions? Curr Oncol Rep 20:34. https://doi.org/10.1007/s11912-018-0682-1

Khan S, Diaz A, Archer KJ et al (2018) Papillary lesions of the breast: to excise or observe? Breast J 24:350–355. https://doi.org/10.1111/tbj.12907

Nayak A, Carkaci S, Gilcrease MZ et al (2013) Benign papillomas without atypia diagnosed on core needle biopsy: experience from a single institution and proposed criteria for excision. Clin Breast Cancer 13:439–449. https://doi.org/10.1016/j.clbc.2013.08.007

Swapp RE, Glazebrook KN, Jones KN et al (2013) Management of benign intraductal solitary papilloma diagnosed on core needle biopsy. Ann Surg Oncol 20:1900–1905. https://doi.org/10.1245/s10434-012-2846-9

Bennett LE, Ghate SV, Bentley R, Baker JA (2010) Is surgical excision of core biopsy proven benign papillomas of the breast necessary? Acad Radiol 17:553–557. https://doi.org/10.1016/j.acra.2010.01.001

Kim MJ, Kim S-I, Youk JH et al (2011) The diagnosis of non-malignant papillary lesions of the breast: comparison of ultrasound-guided automated gun biopsy and vacuum-assisted removal. Clin Radiol 66:530–535. https://doi.org/10.1016/j.crad.2011.01.008

Boufelli G, Giannotti MA, Ruiz CA et al (2018) Papillomas of the breast: factors associated with underestimation. Eur J Cancer 27:310–314. https://doi.org/10.1097/CEJ.0000000000000343

Hong YR, Song BJ, Jung SS, Kang BJ, Kim SH, Chae BJ (2016) Predictive factors for upgrading patients with benign breast papillary lesions using a core needle biopsy. J Breast Cancer 19:410–416. https://doi.org/10.4048/jbc.2016.19.4.410

Kil WH, Cho EY, Kim JH, Nam SJ, Yang JH (2008) Is surgical excision necessary in benign papillary lesions initially diagnosed at core biopsy? Breast 17(3):258–262

Nakhlis F, Ahmadiyeh N, Lester S, Raza S, Lotfi P, Golshan M (2015) Papilloma on core biopsy: excision vs. observation. Ann Surg Oncol 22:1479–1482. https://doi.org/10.1245/s10434-014-4091-x

Youk JH, Kim MJ, Son EJ, Kwak JY, Kim EK (2012) US-guided vacuum-assisted percutaneous excision for management of benign papilloma without atypia diagnosed at US-guided 14-gauge core needle biopsy. Ann Surg Oncol 19:922–928. https://doi.org/10.1245/s10434-011-2033-4

Mosier AD, Keylock J, Smith DV (2013) Benign papillomas diagnosed on large-gauge vacuum-assisted core needle biopsy which span < 1.5 cm do not need surgical excision. Breast J 19:611–617. https://doi.org/10.1111/tbj.12180

Rizzo M, Linebarger J, Lowe MC et al (2012) Management of papillary breast lesions diagnosed on core-needle biopsy: clinical pathologic and radiologic analysis of 276 cases with surgical follow-up. J Am Coll Surg 214:280–287. https://doi.org/10.1016/j.jamcollsurg.2011.12.005

Ciurea A, Calin A, Ciortea C, Dudea SM (2015) Ultrasound in the diagnosis of papillary breast lesions. Med Ultrason 17:392–397. https://doi.org/10.11152/mu.2013.2066.173.aci

Ballesio L, Maggi C, Savelli S et al (2007) Adjunctive diagnostic value of ultrasonography evaluation in patients with suspected ductal breast disease. Radiol Med 112:354–365. https://doi.org/10.1007/s11547-007-0146-4

Hirose M, Nobusawa H, Gokan T (2007) MR ductography: comparison with conventional ductography as a diagnostic method in patients with nipple discharge. Radiogr Rev Publ Radiol Soc N Am Inc 27(Suppl 1):S183–S196. https://doi.org/10.1148/rg.27si075501

Leithner D, Kaltenbach B, Hödl P et al (2018) Intraductal papilloma without atypia on image-guided breast biopsy: upgrade rates to carcinoma at surgical excision. Breast Care 13:364–368. https://doi.org/10.1159/000489096

Magro G, Salvatorelli L, Puzzo L et al (2019) Practical approach to diagnosis of bland-looking spindle cell lesions of the breast. Pathologica 111:344–360. https://doi.org/10.32074/1591-951X-31-19

Charu V, Cimino-Mathews A (2017) Spindle-cell lesions of the breast. AJSP Rev Rep 22:116–123

Rowell MD, Perry RR, Hsiu JG, Barranco SC (1993) Phyllodes tumors. Am J Surg 165:376–379. https://doi.org/10.1016/s0002-9610(05)80849-9

Chua CL, Thomas A, Ng BK (1988) Cystosarcoma phyllodes–Asian variations. Aust N Z J Surg 58:301–305

Tan PH, Thike AA, Tan WJ et al (2012) Predicting clinical behaviour of breast phyllodes tumours: a nomogram based on histological criteria and surgical margins. J Clin Pathol 65:69–76. https://doi.org/10.1136/jclinpath-2011-200368

Sevinç Aİ, Aksoy SÖ, Güray Durak M, Balcı P (2018) Is the extent of surgical resection important in patient outcome in benign and borderline phyllodes tumors of the breast? Turk J Med Sci 48:28–33. https://doi.org/10.3906/sag-1704-47

Mangi AA, Smith BL, Gadd MA, Tanabe KK, Ott MJ, Souba WW (1999) Surgical management of phyllodes tumors. Arch Surg 1960 134:487–492. https://doi.org/10.1001/archsurg.134.5.487

de Roos WK, Kaye P, Dent DM (1999) Factors leading to local recurrence or death after surgical resection of phyllodes tumours of the breast. Br J Surg 86:396–399. https://doi.org/10.1046/j.1365-2168.1999.01035.x

Tan BY, Acs G, Apple SK et al (2016) Phyllodes tumours of the breast: a consensus review. Histopathology 68:5–21. https://doi.org/10.1111/his.12876

Plaza MJ, Swintelski C, Yaziji H, Torres-Salichs M, Esserman LE (2015) Phyllodes tumor: review of key imaging characteristics. Breast Dis 35:79–86. https://doi.org/10.3233/BD-150399

Chao T-C, Lo Y-F, Chen S-C, Chen M-F (2002) Sonographic features of phyllodes tumors of the breast. Ultrasound Obstet Gynecol 20:64–71. https://doi.org/10.1046/j.1469-0705.2002.00736.x

Liberman L, Bonaccio E, Hamele-Bena D, Abramson AF, Cohen MA, Dershaw DD (1996) Benign and malignant phyllodes tumors: mammographic and sonographic findings. Radiology 198:121–124. https://doi.org/10.1148/radiology.198.1.8539362

Cole-Beuglet C, Soriano R, Kurtz AB, Meyer JE, Kopans DB, Goldberg BB (1983) Ultrasound, x-ray mammography, and histopathology of cystosarcoma phylloides. Radiology 146:481–486. https://doi.org/10.1148/radiology.146.2.6294737

Farria DM, Gorczyca DP, Barsky SH, Sinha S, Bassett LW (1996) Benign phyllodes tumor of the breast: MR imaging features. AJR Am J Roentgenol 167:187–189. https://doi.org/10.2214/ajr.167.1.8659370

Kinoshita T, Fukutomi T, Kubochi K (2004) Magnetic resonance imaging of benign phyllodes tumors of the breast. Breast J 10:232–236. https://doi.org/10.1111/j.1075-122X.2004.21316.x

Yabuuchi H, Matsuo Y, Okafuji T et al (2008) Enhanced mass on contrast-enhanced breast MR imaging: lesion characterization using combination of dynamic contrast-enhanced and diffusion-weighted MR images. J Magn Reson Imaging 28:1157–1165. https://doi.org/10.1002/jmri.21570

Ouyang Q, Li S, Tan C et al (2016) Benign phyllodes tumor of the breast diagnosed after ultrasound-guided vacuum-assisted biopsy: surgical excision or wait-and-watch? Ann Surg Oncol 23:1129–1134. https://doi.org/10.1245/s10434-015-4990-5

Youk JH, Kim H, Kim E-K, Son EJ, Kim MJ, Kim JA (2015) Phyllodes tumor diagnosed after ultrasound-guided vacuum-assisted excision: should it be followed by surgical excision? Ultrasound Med Biol 41:741–747. https://doi.org/10.1016/j.ultrasmedbio.2014.11.004