Skip to main content

Advertisement

Log in

Non-classic LCIS Versus Classic LCIS Versus Atypical Hyperplasia: Should Management be the Same?

  • Breast Cancer Surgery (J. Tchou, Section Editor)
  • Published:
Current Surgery Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

This review summarizes the literature from the last 5 years regarding atypical ductal hyperplasia (ADH), atypical lobular hyperplasia (ALH), classic lobular carcinoma in situ (C-LCIS), and non-classic LCIS (NC-LCIS).

Recent Findings

ADH, ALH, and C-LCIS are well-established markers of increased breast cancer risk. Recent studies suggest the possibility of observation for select cases of ADH diagnosed on core biopsy; however, guidelines support routine excision. In contrast, accumulating data support observation for ALH and C-LCIS on core biopsy with radiographic–pathologic concordance. Data on the natural history of pure NC-LCIS remain limited; however, when NC-LCIS is diagnosed on core biopsy, routine excision is warranted.

Summary

ALH and C-LCIS on core biopsy should be reviewed for concordance to determine the need for excision; independent of surgical excision, all warrant counseling regarding increased future breast cancer risk. Current guidelines support routine excision for ADH and NC-LCIS on core biopsy. The natural history of NC-LCIS remains poorly defined.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Chaudhary S, Lawrence L, McGinty G, Kostroff K, Bhuiya T. Classic lobular neoplasia on core biopsy: a clinical and radio-pathologic correlation study with follow-up excision biopsy. Mod Pathol. 2013;26(6):762–71. https://doi.org/10.1038/modpathol.2012.221.

    PubMed  Google Scholar 

  2. Murray MP, Luedtke C, Liberman L, Nehhozina T, Akram M, Brogi E. Classic lobular carcinoma in situ and atypical lobular hyperplasia at percutaneous breast core biopsy: outcomes of prospective excision. Cancer. 2013;119(5):1073–9. https://doi.org/10.1002/cncr.27841.

    PubMed  Google Scholar 

  3. Nakhlis F, Gilmore L, Gelman R, Bedrosian I, Ludwig K, Hwang ES, et al. Incidence of adjacent synchronous invasive carcinoma and/or ductal carcinoma in situ in patients with lobular neoplasia on core biopsy: results from a Prospective Multi-Institutional Registry (TBCRC 020). Ann Surg Oncol. 2016;23(3):722–8. https://doi.org/10.1245/s10434-015-4922-4. This is a prospective multi-institutional single arm trial designed to document upgrade rate of core biopsy diagnoses of atypical lobular hyperplasia and classic lobular carcinoma in situ to malignancy upon excision.

  4. Hoda SA, Brogi E, Koerner FC, Rosen PP, editors. Rosen’s breast pathology. 4th ed. Philadelphia: Lippincott Williams and Wilkins; 2014.

    Google Scholar 

  5. Latronico A, Nicosia L, Faggian A, Abbate F, Penco S, Bozzini A, et al. Atypical ductal hyperplasia: our experience in the management and long term clinical follow-up in 71 patients. Breast. 2017;37:1–5. https://doi.org/10.1016/j.breast.2017.10.003.

    PubMed  Google Scholar 

  6. Nguyen CV, Albarracin CT, Whitman GJ, Lopez A, Sneige N. Atypical ductal hyperplasia in directional vacuum-assisted biopsy of breast microcalcifications: considerations for surgical excision. Ann Surg Oncol. 2011;18(3):752–61. https://doi.org/10.1245/s10434-010-1127-8.

    PubMed  Google Scholar 

  7. Hartmann LC, Degnim AC, Santen RJ, Dupont WD, Ghosh K. Atypical hyperplasia of the breast-risk assessment and management options. N Engl J Med. 2015;372(1):78–89. https://doi.org/10.1056/NEJMsr1407164.

    PubMed  PubMed Central  Google Scholar 

  8. Collins LC, Aroner SA, Connolly JL, Colditz GA, Schnitt SJ, Tamimi RM. Breast cancer risk by extent and type of atypical hyperplasia: an update from the Nurses’ Health Studies. Cancer. 2016;122(4):515–20. https://doi.org/10.1002/cncr.29775.

    PubMed  Google Scholar 

  9. Hartmann LC, Radisky DC, Frost MH, Santen RJ, Vierkant RA, Benetti LL, et al. Understanding the premalignant potential of atypical hyperplasia through its natural history: a longitudinal cohort study. Cancer Prev Res (Phila). 2014;7(2):211–7. https://doi.org/10.1158/1940-6207.CAPR-13-0222.

    CAS  Google Scholar 

  10. Rosen PP. Columnar cell hyperplasia is associated with lobular carcinoma in situ and tubular carcinoma. Am J Surg Pathol. 1999;23(12):1561.

    Article  CAS  PubMed  Google Scholar 

  11. Abdel-Fatah TM, Powe DG, Hodi Z, Lee AH, Reis-Filho JS, Ellis IO. High frequency of coexistence of columnar cell lesions, lobular neoplasia, and low grade ductal carcinoma in situ with invasive tubular carcinoma and invasive lobular carcinoma. Am J Surg Pathol. 2007;31(3):417–26. https://doi.org/10.1097/01.pas.0000213368.41251.b9.

    PubMed  Google Scholar 

  12. Reis-Filho JS, Lakhani SR. The diagnosis and management of pre-invasive breast disease: genetic alterations in pre-invasive lesions. Breast Cancer Res. 2003;5(6):313–9. https://doi.org/10.1186/bcr650.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Brandt SM, Young GQ, Hoda SA. The “Rosen Triad”: tubular carcinoma, lobular carcinoma in situ, and columnar cell lesions. Adv Anat Pathol. 2008;15(3):140–6. https://doi.org/10.1097/PAP.0b013e31816ff313.

    PubMed  Google Scholar 

  14. O’Connell P, Pekkel V, Fuqua SA, Osborne CK, Clark GM, Allred DC. Analysis of loss of heterozygosity in 399 premalignant breast lesions at 15 genetic loci. J Natl Cancer Inst. 1998;90(9):697–703.

    Article  PubMed  Google Scholar 

  15. Simpson PT, Gale T, Reis-Filho JS, Jones C, Parry S, Sloane JP, et al. Columnar cell lesions of the breast: the missing link in breast cancer progression? A morphological and molecular analysis. Am J Surg Pathol. 2005;29(6):734–46.

    Article  PubMed  Google Scholar 

  16. Moinfar F, Man YG, Bratthauer GL, Ratschek M, Tavassoli FA. Genetic abnormalities in mammary ductal intraepithelial neoplasia-flat type (“clinging ductal carcinoma in situ”): a simulator of normal mammary epithelium. Cancer. 2000;88(9):2072–81.

    Article  CAS  PubMed  Google Scholar 

  17. Lakhani SR, Collins N, Stratton MR, Sloane JP. Atypical ductal hyperplasia of the breast: clonal proliferation with loss of heterozygosity on chromosomes 16q and 17p. J Clin Pathol. 1995;48(7):611–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Amari M, Suzuki A, Moriya T, Yoshinaga K, Amano G, Sasano H, et al. LOH analyses of premalignant and malignant lesions of human breast: frequent LOH in 8p, 16q, and 17q in atypical ductal hyperplasia. Oncol Rep. 1999;6(6):1277–80.

    CAS  PubMed  Google Scholar 

  19. Gong G, DeVries S, Chew KL, Cha I, Ljung BM, Waldman FM. Genetic changes in paired atypical and usual ductal hyperplasia of the breast by comparative genomic hybridization. Clin Cancer Res. 2001;7(8):2410–4.

    CAS  PubMed  Google Scholar 

  20. Simpson JF. Update on atypical epithelial hyperplasia and ductal carcinoma in situ. Pathology. 2009;41(1):36–9. https://doi.org/10.1080/00313020802568097.

    PubMed  Google Scholar 

  21. Pinder SE, Ellis IO. The diagnosis and management of pre-invasive breast disease: ductal carcinoma in situ (DCIS) and atypical ductal hyperplasia (ADH)–current definitions and classification. Breast Cancer Res. 2003;5(5):254–7. https://doi.org/10.1186/bcr623.

    PubMed  PubMed Central  Google Scholar 

  22. Martinez AP, Cohen C, Hanley KZ, Li XB. Estrogen receptor and cytokeratin 5 are reliable markers to separate usual ductal hyperplasia from atypical ductal hyperplasia and low-grade ductal carcinoma in situ. Arch Pathol Lab Med. 2016;140(7):686–9. https://doi.org/10.5858/arpa.2015-0238-OA.

    PubMed  Google Scholar 

  23. Elmore JG, Pepe MS, Weaver DL. Discordant interpretations of breast biopsy specimens by pathologists—Reply. JAMA. 2015;314(1):83–4. https://doi.org/10.1001/jama.2015.6239.

    CAS  PubMed  Google Scholar 

  24. Allison KH, Rendi MH, Peacock S, Morgan T, Elmore JG, Weaver DL. Histological features associated with diagnostic agreement in atypical ductal hyperplasia of the breast: illustrative cases from the B-Path study. Histopathology. 2016;69(6):1028–46. https://doi.org/10.1111/his.13035.

    PubMed  PubMed Central  Google Scholar 

  25. Jackman RJ, Burbank F, Parker SH, Evans WP 3rd, Lechner MC, Richardson TR, et al. Atypical ductal hyperplasia diagnosed at stereotactic breast biopsy: improved reliability with 14-gauge, directional, vacuum-assisted biopsy. Radiology. 1997;204(2):485–8. https://doi.org/10.1148/radiology.204.2.9240540.

    CAS  PubMed  Google Scholar 

  26. Eby PR, Ochsner JE, DeMartini WB, Allison KH, Peacock S, Lehman CD. Frequency and upgrade rates of atypical ductal hyperplasia diagnosed at stereotactic vacuum-assisted breast biopsy: 9-versus 11-gauge. AJR Am J Roentgenol. 2009;192(1):229–34. https://doi.org/10.2214/AJR.08.1342.

    PubMed  Google Scholar 

  27. Hoang JK, Hill P, Cawson JN. Can mammographic findings help discriminate between atypical ductal hyperplasia and ductal carcinoma in situ after needle core biopsy? Breast. 2008;17(3):282–8. https://doi.org/10.1016/j.breast.2007.10.016.

    PubMed  Google Scholar 

  28. Kohr JR, Eby PR, Allison KH, DeMartini WB, Gutierrez RL, Peacock S, et al. Risk of upgrade of atypical ductal hyperplasia after stereotactic breast biopsy: effects of number of foci and complete removal of calcifications. Radiology. 2010;255(3):723–30. https://doi.org/10.1148/radiol.09091406.

    PubMed  Google Scholar 

  29. Menen RS, Ganesan N, Bevers T, Ying J, Coyne R, Lane D, et al. Long-term safety of observation in selected women following core biopsy diagnosis of atypical ductal hyperplasia. Ann Surg Oncol. 2017;24(1):70–6. https://doi.org/10.1245/s10434-016-5512-9.

    PubMed  Google Scholar 

  30. Menes TS, Kerlikowske K, Lange J, Jaffer S, Rosenberg R, Miglioretti DL. Subsequent breast cancer risk following diagnosis of atypical ductal hyperplasia on needle biopsy. JAMA Oncol. 2017;3(1):36–41. https://doi.org/10.1001/jamaoncol.2016.3022.

    PubMed  PubMed Central  Google Scholar 

  31. McGhan LJ, Pockaj BA, Wasif N, Giurescu ME, McCullough AE, Gray RJ. Atypical ductal hyperplasia on core biopsy: an automatic trigger for excisional biopsy? Ann Surg Oncol. 2012;19(10):3264–9. https://doi.org/10.1245/s10434-012-2575-0.

    PubMed  Google Scholar 

  32. Dominici L, Liao GS, Brock J, Iglehart JD, Lotfi P, Meyer J, et al. Large needle core biopsy of atypical ductal hyperplasia: results of surgical excision. Breast J. 2012;18(5):506–8. https://doi.org/10.1111/j.1524-4741.2012.01296.x.

    PubMed  Google Scholar 

  33. Renshaw AA, Gould EW. Long term clinical follow-up of atypical ductal hyperplasia and lobular carcinoma in situ in breast core needle biopsies. Pathology. 2016;48(1):25–9. https://doi.org/10.1016/j.pathol.2015.11.015.

    PubMed  Google Scholar 

  34. Mooney KL, Bassett LW, Apple SK. Upgrade rates of high-risk breast lesions diagnosed on core needle biopsy: a single-institution experience and literature review. Mod Pathol. 2016;29(12):1471–84. https://doi.org/10.1038/modpathol.2016.127.

    CAS  PubMed  Google Scholar 

  35. Polat AK, Soran A, Kanbour-Shakir A, Menekse E, Levent Balci F, Johnson R. The role of molecular biomarkers for predicting adjacent breast cancer of Atypical Ductal Hyperplasia diagnosed on core biopsy. Cancer Biomark. 2016;17(3):293–300. https://doi.org/10.3233/CBM-160641.

    CAS  PubMed  Google Scholar 

  36. Fisher B, Costantino JP, Wickerham DL, Cecchini RS, Cronin WM, Robidoux A, et al. Tamoxifen for the prevention of breast cancer: current status of the National Surgical Adjuvant Breast and Bowel Project P-1 study. J Natl Cancer Inst. 2005;97(22):1652–62. https://doi.org/10.1093/jnci/dji372.

    CAS  PubMed  Google Scholar 

  37. Vogel VG, Costantino JP, Wickerham DL, Cronin WM, Cecchini RS, Atkins JN, et al. Update of the National Surgical Adjuvant Breast and Bowel Project Study of Tamoxifen and Raloxifene (STAR) P-2 trial: preventing breast cancer. Cancer Prev Res (Phila). 2010;3(6):696–706. https://doi.org/10.1158/1940-6207.CAPR-10-0076.

    CAS  Google Scholar 

  38. Goss PE, Ingle JN, Ales-Martinez JE, Cheung AM, Chlebowski RT, Wactawski-Wende J, et al. Exemestane for breast-cancer prevention in postmenopausal women. N Engl J Med. 2011;364(25):2381–91. https://doi.org/10.1056/NEJMoa1103507.

    CAS  PubMed  Google Scholar 

  39. Cuzick J, Sestak I, Forbes JF, Dowsett M, Knox J, Cawthorn S, et al. Anastrozole for prevention of breast cancer in high-risk postmenopausal women (IBIS-II): an international, double-blind, randomised placebo-controlled trial. Lancet. 2014;383(9922):1041–8. https://doi.org/10.1016/S0140-6736(13)62292-8.

    CAS  PubMed  Google Scholar 

  40. Bevers T, Ward JH, Arun B, Colditz G, Cowan KH, Daly M, et al. NCCN Breast Cancer Risk Reduction Guidelines, version 1.2017. National Comprehensive Cancer Network; 2017. https://www.nccn.org/professionals/physician_gls/pdf/breast_risk.pdf.

  41. Rosen P. Lobular carcinoma in situ and atypical lobular hyperplasia. Rosen’s breast pathology. 2nd ed. Philadelphia: Lippincott Williams and Wilkin; 2001. p. 581–618.

    Google Scholar 

  42. Beute BJ, Kalisher L, Hutter RV. Lobular carcinoma in situ of the breast: clinical, pathologic, and mammographic features. AJR Am J Roentgenol. 1991;157(2):257–65. https://doi.org/10.2214/ajr.157.2.1853802.

    CAS  PubMed  Google Scholar 

  43. Bauer VP, Ditkoff BA, Schnabel F, Brenin D, El-Tamer M, Smith S. The management of lobular neoplasia identified on percutaneous core breast biopsy. Breast J. 2003;9(1):4–9.

    Article  PubMed  Google Scholar 

  44. 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(3):813–9. https://doi.org/10.1148/radiol.2313030874.

    PubMed  Google Scholar 

  45. Liberman L, Sama M, Susnik B, Rosen PP, LaTrenta LR, Morris EA, et al. Lobular carcinoma in situ at percutaneous breast biopsy: surgical biopsy findings. AJR Am J Roentgenol. 1999;173(2):291–9. https://doi.org/10.2214/ajr.173.2.10430122.

    CAS  PubMed  Google Scholar 

  46. O’Driscoll D, Britton P, Bobrow L, Wishart GC, Sinnatamby R, Warren R. Lobular carcinoma in situ on core biopsy—what is the clinical significance? Clin Radiol. 2001;56(3):216–20. https://doi.org/10.1053/crad.2000.0615.

    PubMed  Google Scholar 

  47. Foote FW, Stewart FW. Lobular carcinoma in situ: a rare form of mammary cancer. Am J Pathol. 1941;17(4):491–496.3.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Haagensen CD, Lane N, Lattes R, Bodian C. Lobular neoplasia (so-called lobular carcinoma in situ) of the breast. Cancer. 1978;42(2):737–69.

    Article  CAS  PubMed  Google Scholar 

  49. Ho BC, Tan PH. Lobular neoplasia of the breast: 68 years on. Pathology. 2009;41(1):28–35. https://doi.org/10.1080/00313020802563494.

    PubMed  Google Scholar 

  50. Mohsin SK, O’Connell P, Allred DC, Libby AL. Biomarker profile and genetic abnormalities in lobular carcinoma in situ. Breast Cancer Res Treat. 2005;90(3):249–56. https://doi.org/10.1007/s10549-004-4493-8.

    PubMed  Google Scholar 

  51. Berx G, Cleton-Jansen AM, Nollet F, de Leeuw WJ, van de Vijver M, Cornelisse C, et al. E-cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers. EMBO J. 1995;14(24):6107–15.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Berx G, Cleton-Jansen AM, Strumane K, de Leeuw WJ, Nollet F, van Roy F, et al. E-cadherin is inactivated in a majority of invasive human lobular breast cancers by truncation mutations throughout its extracellular domain. Oncogene. 1996;13(9):1919–25.

    CAS  PubMed  Google Scholar 

  53. Vos CB, Cleton-Jansen AM, Berx G, de Leeuw WJ, ter Haar NT, van Roy F, et al. E-cadherin inactivation in lobular carcinoma in situ of the breast: an early event in tumorigenesis. Br J Cancer. 1997;76(9):1131–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Berx G, Van Roy F. The E-cadherin/catenin complex: an important gatekeeper in breast cancer tumorigenesis and malignant progression. Breast Cancer Res. 2001;3(5):289–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. •• Ciriello G, Gatza ML, Beck AH, Wilkerson MD, Rhie SK, Pastore A, et al. Comprehensive molecular portraits of invasive lobular breast cancer. Cell. 2015;163(2):506–19. https://doi.org/10.1016/j.cell.2015.09.033. This paper presents a comprehensive molecular description of invasive lobular carcinomas, providing insights into pathogenesis of invasive lobular carcinoma.

  56. • Dabbs DJ, Schnitt SJ, Geyer FC, Weigelt B, Baehner FL, Decker T, et al. Lobular neoplasia of the breast revisited with emphasis on the role of E-cadherin immunohistochemistry. Am J Surg Pathol. 2013;37(7):e1-11. https://doi.org/10.1097/pas.0b013e3182918a2b. Review article from an international group of academic breast pathologists regarding the appropriate application and interpretation of E-cadherin immunohistochemistry in the diagnosis of lobular neoplasia and invasive lobular carcinoma.

  57. Canas-Marques R, Schnitt SJ. E-cadherin immunohistochemistry in breast pathology: uses and pitfalls. Histopathology. 2016;68(1):57–69. https://doi.org/10.1111/his.12869.

    PubMed  Google Scholar 

  58. Lu YJ, Osin P, Lakhani SR, Di Palma S, Gusterson BA, Shipley JM. Comparative genomic hybridization analysis of lobular carcinoma in situ and atypical lobular hyperplasia and potential roles for gains and losses of genetic material in breast neoplasia. Cancer Res. 1998;58(20):4721–7.

    CAS  PubMed  Google Scholar 

  59. Etzell JE, Devries S, Chew K, Florendo C, Molinaro A, Ljung BM, et al. Loss of chromosome 16q in lobular carcinoma in situ. Hum Pathol. 2001;32(3):292–6. https://doi.org/10.1053/hupa.2001.22759.

    CAS  PubMed  Google Scholar 

  60. Hwang ES, Nyante SJ, Yi Chen Y, Moore D, DeVries S, Korkola JE, et al. Clonality of lobular carcinoma in situ and synchronous invasive lobular carcinoma. Cancer. 2004;100(12):2562–72. https://doi.org/10.1002/cncr.20273.

    PubMed  Google Scholar 

  61. • Begg CB, Ostrovnaya I, Carniello JV, Sakr RA, Giri D, Towers R, et al. Clonal relationships between lobular carcinoma in situ and other breast malignancies. Breast Cancer Res. 2016;18(1):66. https://doi.org/10.1186/s13058-016-0727-z. This paper employs whole exome sequencing and CGH arrays to examine the frequency of clonal relatedness between synchronous LCIS and ILC.

  62. Andrade VP, Morrogh M, Qin LX, Olvera N, Giri D, Muhsen S, et al. Gene expression profiling of lobular carcinoma in situ reveals candidate precursor genes for invasion. Mol Oncol. 2015;9(4):772–82. https://doi.org/10.1016/j.molonc.2014.12.005.

    CAS  PubMed  Google Scholar 

  63. • Sakr RA, Schizas M, Carniello JV, Ng CK, Piscuoglio S, Giri D, et al. Targeted capture massively parallel sequencing analysis of LCIS and invasive lobular cancer: Repertoire of somatic genetic alterations and clonal relationships. Mol Oncol. 2016;10(2):360–70. https://doi.org/10.1016/j.molonc.2015.11.001. Targeted capture massively parallel sequencing analysis demonstrated clonal relatedness and overlap in mutational spectra between synchronous ipsilateral LCIS and invasive lobular carcinoma, proving further support that LCIS is a non-obligate precursor lesion.

  64. Renshaw AA, Cartagena N, Derhagopian RP, 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(5):797–9. https://doi.org/10.1309/T4XF-C61J-C95Y-VR4Q.

    PubMed  Google Scholar 

  65. Dmytrasz K, Tartter PI, Mizrachy H, Chinitz L, Rosenbaum Smith S, Estabrook A. The significance of atypical lobular hyperplasia at percutaneous breast biopsy. Breast J. 2003;9(1):10–2.

    Article  PubMed  Google Scholar 

  66. Middleton LP, Grant S, Stephens T, Stelling CB, Sneige N, Sahin AA. Lobular carcinoma in situ diagnosed by core needle biopsy: when should it be excised? Mod Pathol. 2003;16(2):120–9. https://doi.org/10.1097/01.MP.0000051930.68104.92.

    PubMed  Google Scholar 

  67. Arpino G, Allred DC, Mohsin SK, Weiss HL, Conrow D, Elledge RM. Lobular neoplasia on core-needle biopsy—clinical significance. Cancer. 2004;101(2):242–50. https://doi.org/10.1002/cncr.20318.

    PubMed  Google Scholar 

  68. Cangiarella J, Guth A, Axelrod D, Darvishian F, Singh B, Simsir A, et al. Is surgical excision necessary for the management of atypical lobular hyperplasia and lobular carcinoma in situ diagnosed on core needle biopsy?: a report of 38 cases and review of the literature. Arch Pathol Lab Med. 2008;132(6):979–83. https://doi.org/10.1043/1543-2165(2008)132[979:ISENFT]2.0.CO;2.

  69. Shah-Khan MG, Geiger XJ, Reynolds C, Jakub JW, Deperi ER, Glazebrook KN. Long-term follow-up of lobular neoplasia (atypical lobular hyperplasia/lobular carcinoma in situ) diagnosed on core needle biopsy. Ann Surg Oncol. 2012;19(10):3131–8. https://doi.org/10.1245/s10434-012-2534-9.

    PubMed  Google Scholar 

  70. • King TA, Pilewskie M, Muhsen S, Patil S, Mautner SK, Park A, et al. Lobular carcinoma in situ: a 29-year longitudinal experience evaluating clinicopathologic features and breast cancer risk. J Clin Oncol. 2015;33(33):3945–52. https://doi.org/10.1200/jco.2015.61.4743. This paper describes the natural history of lobular carcinoma in situ over a 29-year clinical follow-up period and emphasizes the importance of appropriate patient counseling regarding chemoprevention.

  71. Frost AR, Tsangaris TN, Silverberg SG. Pleomorphic lobular carcinoma in situ. Pathol Case Rev. 1996;1:27–30.

    Article  Google Scholar 

  72. Sneige N, Wang J, Baker BA, Krishnamurthy S, Middleton LP. Clinical, histopathologic, and biologic features of pleomorphic lobular (ductal-lobular) carcinoma in situ of the breast: a report of 24 cases. Mod Pathol. 2002;15(10):1044–50. https://doi.org/10.1097/01.MP.0000027624.08159.19.

    PubMed  Google Scholar 

  73. Lakhani SR, Ellis IO, Schnitt SJ, Tan PH, Van de Vijver M. WHO classification of tumours of the breast. 4th ed. Lyon: IARC Press; 2012. p. 240.

    Google Scholar 

  74. Fadare O, Dadmanesh F, Alvarado-Cabrero I, Snyder R, Stephen Mitchell J, Tot T, et al. Lobular intraepithelial neoplasia [lobular carcinoma in situ] with comedo-type necrosis: a clinicopathologic study of 18 cases. Am J Surg Pathol. 2006;30(11):1445–53. https://doi.org/10.1097/01.pas.0000213290.58283.82.

    PubMed  Google Scholar 

  75. Alvarado-Cabrero I, Picon Coronel G, Valencia Cedillo R, Canedo N, Tavassoli FA. Florid lobular intraepithelial neoplasia with signet ring cells, central necrosis and calcifications: a clinicopathological and immunohistochemical analysis of ten cases associated with invasive lobular carcinoma. Arch Med Res. 2010;41(6):436–41. https://doi.org/10.1016/j.arcmed.2010.08.010.

    PubMed  Google Scholar 

  76. Tavassoli FA. Lobular neoplasia: evolution of its significance and morphologic spectrum. Int J Surg Pathol. 2010;18(3 Suppl):174S–7S. https://doi.org/10.1177/1066896910370879.

    PubMed  Google Scholar 

  77. Shin SJ, Lal A, De Vries S, Suzuki J, Roy R, Hwang ES, et al. Florid lobular carcinoma in situ: molecular profiling and comparison to classic lobular carcinoma in situ and pleomorphic lobular carcinoma in situ. Hum Pathol. 2013;44(10):1998–2009. https://doi.org/10.1016/j.humpath.2013.04.004.

    CAS  PubMed  Google Scholar 

  78. Murray M, Brogi E. Lobular carcinoma in situ, classical type and unusual variants. Surg Pathol Clin. 2009;2(2):273–99. https://doi.org/10.1016/j.path.2009.02.001.

    PubMed  Google Scholar 

  79. Ginter PS, D’Alfonso TM. 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. 2017;141(12):1668–78. https://doi.org/10.5858/arpa.2016-0421-RA.

    PubMed  Google Scholar 

  80. Tan PH, Harada O, Thike AA, Tse GM. Histiocytoid breast carcinoma: an enigmatic lobular entity. J Clin Pathol. 2011;64(8):654–9. https://doi.org/10.1136/jcp.2011.088930.

    PubMed  Google Scholar 

  81. Fadare O. Pleomorphic lobular carcinoma in situ of the breast composed almost entirely of signet ring cells. Pathol Int. 2006;56(11):683–7. https://doi.org/10.1111/j.1440-1827.2006.02030.x.

    PubMed  Google Scholar 

  82. Chen YY, Hwang ES, Roy R, DeVries S, Anderson J, Wa C, et al. Genetic and phenotypic characteristics of pleomorphic lobular carcinoma in situ of the breast. Am J Surg Pathol. 2009;33(11):1683–94. https://doi.org/10.1097/PAS.0b013e3181b18a89.

    PubMed  PubMed Central  Google Scholar 

  83. Gomes DS, Porto SS, Balabram D, Gobbi H. Inter-observer variability between general pathologists and a specialist in breast pathology in the diagnosis of lobular neoplasia, columnar cell lesions, atypical ductal hyperplasia and ductal carcinoma in situ of the breast. Diagn Pathol. 2014;9:121. https://doi.org/10.1186/1746-1596-9-121.

    PubMed  PubMed Central  Google Scholar 

  84. Georgian-Smith D, Lawton TJ. Calcifications of lobular carcinoma in situ of the breast: radiologic-pathologic correlation. AJR Am J Roentgenol. 2001;176(5):1255–9. https://doi.org/10.2214/ajr.176.5.1761255.

    CAS  PubMed  Google Scholar 

  85. Lavoue V, Graesslin O, Classe JM, Fondrinier E, Angibeau H, Leveque J. Management of lobular neoplasia diagnosed by core needle biopsy: study of 52 biopsies with follow-up surgical excision. Breast. 2007;16(5):533–9. https://doi.org/10.1016/j.breast.2007.04.005.

    PubMed  Google Scholar 

  86. Chivukula M, Haynik DM, Brufsky A, Carter G, Dabbs DJ. Pleomorphic lobular carcinoma in situ (PLCIS) on breast core needle biopsies: clinical significance and immunoprofile. Am J Surg Pathol. 2008;32(11):1721–6. https://doi.org/10.1097/PAS.0b013e31817dc3a6.

    PubMed  Google Scholar 

  87. Carder PJ, Shaaban A, Alizadeh Y, Kumarasuwamy V, Liston JC, Sharma N. Screen-detected pleomorphic lobular carcinoma in situ (PLCIS): risk of concurrent invasive malignancy following a core biopsy diagnosis. Histopathology. 2010;57(3):472–8. https://doi.org/10.1111/j.1365-2559.2010.03634.x.

    PubMed  Google Scholar 

  88. Niell B, Specht M, Gerade B, Rafferty E. Is excisional biopsy required after a breast core biopsy yields lobular neoplasia? AJR Am J Roentgenol. 2012;199(4):929–35. https://doi.org/10.2214/AJR.11.8447.

    PubMed  Google Scholar 

  89. Meroni S, Bozzini AC, Pruneri G, Moscovici OC, Maisonneuve P, Menna S, et al. Underestimation rate of lobular intraepithelial neoplasia in vacuum-assisted breast biopsy. Eur Radiol. 2014;24(7):1651–8. https://doi.org/10.1007/s00330-014-3132-y.

    PubMed  Google Scholar 

  90. Flanagan MR, Rendi MH, Calhoun KE, Anderson BO, Javid SH. Pleomorphic lobular carcinoma in situ: radiologic-pathologic features and clinical management. Ann Surg Oncol. 2015;22(13):4263–9. https://doi.org/10.1245/s10434-015-4552-x.

    PubMed  PubMed Central  Google Scholar 

  91. Nakhlis F, Harrison BT, Lester S, Hughes KS, Coopey SB, King TA. Evaluating the risk of upgrade to invasive breast cancer and/or DCIS on excision following a diagnosis of non-classic lobular carcinoma in situ. [Poster at San Antonio Breast Cancer Symposium, San Antonio, TX] (2017).

  92. Susnik B, Day D, Abeln E, Bowman T, Krueger J, Swenson KK, et al. Surgical outcomes of lobular neoplasia diagnosed in core biopsy: prospective study of 316 cases. Clin Breast Cancer. 2016;16(6):507–13. https://doi.org/10.1016/j.clbc.2016.06.003.

    PubMed  Google Scholar 

  93. Guo T, Wang Y, Shapiro N, Fineberg S. Pleomorphic lobular carcinoma in situ diagnosed by breast core biopsy: clinicopathologic features and correlation with subsequent excision. Clin Breast Cancer. 2017. https://doi.org/10.1016/j.clbc.2017.10.004.

    Google Scholar 

  94. Downs-Kelly E, Bell D, Perkins GH, Sneige N, Middleton LP. Clinical implications of margin involvement by pleomorphic lobular carcinoma in situ. Arch Pathol Lab Med. 2011;135(6):737–43. https://doi.org/10.1043/2010-0204-OA.1.

    PubMed  Google Scholar 

  95. De Brot M, Koslow Mautner S, Muhsen S, Andrade VP, Mamtani A, Murray M, et al. Pleomorphic lobular carcinoma in situ of the breast: a single institution experience with clinical follow-up and centralized pathology review. Breast Cancer Res Treat. 2017;165(2):411–20. https://doi.org/10.1007/s10549-017-4334-1.

    PubMed  Google Scholar 

  96. Khoury T, Karabakhtsian RG, Mattson D, Yan L, Syriac S, Habib F, et al. Pleomorphic lobular carcinoma in situ of the breast: clinicopathological review of 47 cases. Histopathology. 2014;64(7):981–93. https://doi.org/10.1111/his.12353.

    PubMed  PubMed Central  Google Scholar 

  97. Bevers T, Helvie M, Bonaccio E, Calhoun KE, Daly M, Farrar W, et al. NCCN Breast Cancer Screening and Diagnosis Guidelines, version 1.2017. National Comprehensive Cancer Network; 2017. https://www.nccn.org/professionals/physician_gls/PDF/breast-screening.pdf.

  98. Saslow D, Boetes C, Burke W, Harms S, Leach MO, Lehman CD, et al. American Cancer Society guidelines for breast screening with MRI as an adjunct to mammography. CA Cancer J Clin. 2007;57(2):75–89.

    Article  PubMed  Google Scholar 

  99. King TA, Muhsen S, Patil S, Koslow S, Oskar S, Park A, et al. Is there a role for routine screening MRI in women with LCIS? Breast Cancer Res Treat. 2013;142(2):445–53. https://doi.org/10.1007/s10549-013-2725-5.

    PubMed  Google Scholar 

  100. Gail MH, Brinton LA, Byar DP, Corle DK, Green SB, Schairer C, et al. Projecting individualized probabilities of developing breast cancer for white females who are being examined annually. J Natl Cancer Inst. 1989;81(24):1879–86.

    Article  CAS  PubMed  Google Scholar 

  101. Cuzick J. Preventive therapy for cancer. Lancet Oncol. 2017;18(8):e472–82. https://doi.org/10.1016/S1470-2045(17)30536-3.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tari A. King.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest relevant to this manuscript.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

This article is part of the Topical collection on Breast Cancer Surgery.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nakhlis, F., Harrison, B.T. & King, T.A. Non-classic LCIS Versus Classic LCIS Versus Atypical Hyperplasia: Should Management be the Same?. Curr Surg Rep 6, 2 (2018). https://doi.org/10.1007/s40137-018-0201-1

Download citation

  • Published:

  • DOI: https://doi.org/10.1007/s40137-018-0201-1

Keywords

Navigation